Взаимосвязь когнитивного и моторного развития у детей с нарушением двигательной активности тема диссертации и автореферата по ВАК РФ 00.00.00, кандидат наук Корякина Мария Михайловна

• Корякина Мария Михайловна
• кандидат наук
• 2024

Оглавление диссертации кандидат наук Корякина Мария Михайловна

.1. Проблема исследования

.2. Цели и задачи исследования

.3. Методология и дизайн исследования

.4. Научная новизна

.5. Методологическая новизна

.6. Эмпирическая новизна

.7. Положения, выносимые на защиту

.8. Вклад автора

2. ОПИСАНИЕ ИССЛЕДОВАНИЙ

2.1. Исследование 1. Исследование когнитивных особенностей детей с моторными нарушениями

2.2. Исследование 2. Исследования различий когнитивных функций детей с моторными заболеваниями и здоровых детей

2.3. Исследование 3. Исследование нейрональных коррелятов восприятия движений с применением ЭЭГ

3. ЗАКЛЮЧЕНИЕ

СПИСОК ЛИТЕРАТУРЫ

ПРИЛОЖЕНИЕ А. Статья «Aberrant Auditory and Visual Memory Development of Children with Upper Limb Motor Disorders»

ПРИЛОЖЕНИЕ Б. Статья «Similar Cognitive Skill Impairment in Children with Upper Limb Motor Disorders Due to Arthrogryposis Multiplex Congenita and Obstetrical Brachial Plexus Palsy»

ПРИЛОЖЕНИЕ В. Статья «Developmental differences in the perception of naturalistic human movements»

ПРИЛОЖЕНИЕ Г. Статья «Altered Cerebral Processing of Videos in Children with Motor Dysfunction Suggests Broad Embodiment of Perceptual Cognitive Functions»

Работа выполнена в Центре нейроэкономики и когнитивных исследований Национального исследовательского университета «Высшая школа экономики».

Основные результаты диссертационного исследования представлены в следующих публикациях:

Публикации первого уровня1

A. Blagovechtchenski, E., Koriakina, M., Bredikhin, D., Agranovich, O., Kadieva, D., Ermolovich, E., ... & Shestakova, A. N..Similar Cognitive Skill Impairment in Children with Upper Limb Motor Disorders Due to Arthrogryposis Multiplex Congenita and Obstetrical Brachial Plexus Palsy //International Journal of Environmental Research and Public Health. - 2023. - Т. 20. - №. 3. - С

Б. Ntoumanis, I., Shestakova, A., Koriakina, M., Kadieva, D., Kopytin, G., & Jaaskelainen, I. P. (2023). Developmental differences in the perception of naturalistic human movements. Frontiers in Human Neuroscience, 16,

B. Ntoumanis I, Agranovich O, Shestakova AN, Blagovechtchenski E, Koriakina M, Kadieva D, Kopytin G, Jaaskelainen IP. Altered Cerebral Processing of Videos in Children with Motor Dysfunction Suggests Broad Embodiment of Perceptual Cognitive Functions. J Pers Med. 2022 Nov 4;12(11): 1841. doi: 10.3390/jpm12111841. PMID: 36579567; PMCID: PMC9697218.

1 К публикациям первого уровня относятся статьи, индексируемые в базах данных Web of

Science (Q1 или Q2) или Scopus (Q1 или Q2), а также рецензируемые сборники конференций, которые появляются в рейтингах CORE (ранги A и A*).

Публикации второго уровня2

Г. Maria Koriakina, Olga Agranovich, Ekaterina Petrova, Dzerassa Kadieva, Grigory Kopytin, Evgenia Ermolovich, Olesya Moiseenko, Margarita Alekseeva, Dimitri Bredikhin, Beatriz Bermüdez-Margaretto, Ioannis Ntoumanis, Anna N Shestakova, Iiro P Jääskeläinen, Evgeny Blagovechtchenski. Aberrant auditory and visual memory development of children with upper limb motor disorders //Brain Sciences. - 2021. - Т. 11. -№. 12. - С

Доклады о конференциях

А. Koriakina, M., Agranovich, O., Bermüdez-Margaretto, B., Ulanov, M., Shestakova, A., & Blagovechtchenski, E. (2022, September). Relationship Between Motor Impairments And Verbal Fluency In Children. In 2022 Fourth International Conference Neurotechnologies and Neurointerfaces (CNN) (pp. 78-81). IEEE.

Б. Koriakina, M., Agranovich, O., Bermüdez-Margaretto, B., Ulanov, M., Shestakova, A., & Blagovechtchenski, E. (2023, September). Verbal Fluency and Semantic Association Deficits in Children with Upper Limb Motor Disorders. In 2023 Fifth International Conference Neurotechnologies and Neurointerfaces (CNN) (pp. 1-5). IEEE.

2021 Межрегиональная научно-практическая конференция «Современные методики реабилитации двигательных нарушений у детей» с презентацией на

2 К изданиям второго уровня относятся статьи, опубликованные в журналах, входящих в

перечень высококачественных журналов НИУ ВШЭ или индексируемых в базах данных Web of Science (Q3 или Q4) или Scopus (Q3 или Q4), а также рецензируемые сборники конференций, входящие в рейтинг CORE (ранг B).

тему «Динамика ЭЭГ как показатель эффективности реабилитации у детей с артрогрипозом»

2022 CNN'2022, Четвертая международная конференция "Нейротехнологии и нейроинтерфейсы», с презентацией на тему: «Relationship Between Motor Impairments And Verbal Fluency In Children»

2022 III Объединенный научный форум физиологов, биохимиков и молекулярных Биологов, с презентацией на тему: «Особенности взаимосвязи между развитием речи и когнитивным развитием у детей с нарушениями верхних конечностей (артрогрипоз)»

2022 Конференция «Современные возможности нейротехнологий в диагностике и лечении тяжелых моторных нарушений у детей» в «НМИЦ детской травматологии и ортопедии имени Г.И. Турнера» с докладом на тему «Нарушение когнитивных навыков у детей с моторными расстройствами»

2023 CNN'2023, Пятая международная конференция "Нейротехнологии и нейроинтерфейсы», с презентацией на тему: «Verbal Fluency and Semantic Association Deficits in Children with Upper Limb Motor Disorders»

2023 "International Conference on Biomedical Science and Engineering", с презентацией на тему «Impact of Upper Extremity Motor Impairments on Cognitive Processes and Perception in Children»

Работа проводилась в Центре нейроэкономики и когнитивных исследований Института когнитивных нейронаук Национального исследовательского университета «Высшая школа экономики», Москва, Российская Федерация, а также в федеральном государственном бюджетном учреждении Национальный медицинский исследовательский центр детской травматологии и ортопедии имени Г.И. Турнера.

Список сокращений

ЭЭГ - электроэнцефалография

МЭГ - Магнитоэнцефалография

ERP - потенциал вызванного отклика

ISC - межсубъектный корреляционный анализ

FDR - частота ложного обнаружения

Введение диссертации (часть автореферата) на тему «Взаимосвязь когнитивного и моторного развития у детей с нарушением двигательной активности»

1. ВВЕДЕНИЕ

1.1. Проблема исследования

Взаимосвязь между когнитивным и моторным развитием давно является предметом внимания психологии и психофизиологии, тем не менее, этот вопрос до сих пор остается дискуссионным, т.к. нейрональные механизмы, лежащие в основе этой связи всё ещё не понятны (Hauert, 1986; Iverson, 2010; Van der Fels и др., 2015; Martzog и др., 2019). Целью данной работы было исследование взаимосвязи моторных и когнитивных функций у детей с нарушением развития верхних конечностей.

Степень разработанности темы. Исследования указывают на взаимосвязь между некоторыми категориями моторных и когнитивных функций (Stein et al., 2017; Invernizzi P. L. et al.; Hama et al., 2020; Stöckel and Hughes, 2016; Marvel et al., 2019). Так, в недавнем исследовании было показано, что увеличение физической нагрузки детей в младшем школьном возрасте улучшает не только моторные навыки, но и когнитивные способности, связанные с успеваемостью детей в школе (Ferreira Vorkapic и др., 2021). Другие исследования показали, что развитие локомоции и общего контроля над телом расширяет потенциальную сферу опыта и способствует развитию исследовательской деятельности ребенка (Stöckel и Hughes, 2016).

Имеются исследования в которых было обнаружено, что у детей среднего дошкольного возраста наблюдается более выраженная связь между моторными и когнитивными навыками по сравнению с детьми старшего школьного возраста (Van der Fels и др., 2015), это означает что в разные этапы развития ребенка могут проявляться различные формы взаимодействия этих двух функций, и этот вопрос имеет важное прикладное значение.

В нашем исследовании приняли участие дети с нарушениями двигательной функции верхних конечностей, и по этому важным представляется рассмотреть отдельно влияние мелкой моторики на когнитивные функции. Мелкая моторика представляет собой совокупность скоординированных действий различных систем организма и задействуется в процессе выполнении мелких и точных движений кистями рук и пальцами рук и ног (Martzog и др., 2019).

Исследования показали, что пальцы руки имеют обширное представительство в коре больших полушарий мозга (Shapiro, 2019; Tardelli и др., 2022). Развитие движений пальцев рук предшествует появлению артикуляции слогов, и уровень развития моторики связан с качеством артикуляции ребенка (Sullivan, 2018.). Более того, благодаря моторному развитию пальцев, в мозгу формируется проекция «схемы человеческого тела», и речевые реакции находятся в прямой зависимости от тренировки пальцев (Виноградова, 2009; Naito и др., 2017).

Процессы, лежащие в основе этих взаимодействий, формируются на ранних стадиях развития ребенка. Важно отметить, что развивающаяся двигательная система, позволяющая ребенку точно управлять мышцами, необходимыми для того или иного движения, дает средства для эффективного взаимодействия с окружающей средой, и при отсутствии таких навыков ребенок привыкает к тому, что все функции такого взаимодействия выполняет его родитель (Houwen и др., 2016), что впоследствии сказывается на восстановлении ребенка в процессе реабилитации.

Доказательства тесной связи между когнитивным и моторным развитием не ограничиваются поведенческой областью. Также нейрофизиологические исследования выявили совместную активацию структур мозга,

ассоциирующихся с моторными и когнитивными функциями мозга. Например, связанная активация мозжечка, базальных ганглиев и префронтальной коры были показаны во время выполнения различных двигательных и когнитивных задач, особенно сложных, новых, с меняющимися условиями или требующих быстрой реакции и концентрации внимания (Davis, 2009; Salman, 2016).

В воспроизведении движения задействована ретикулярная формация, префронтальная кора, а также базальные ганглии. Они, взаимодействуя с лобными долями, корой больших полушарий, таламусом, лимбической системой и стволом головного мозга, обеспечивают контроль над движениями и устанавливают функциональные связи с проводящими образованиями и мозжечком, ретранслируя информацию обратно в кору (Bugalho et al., 2006).

Таким образом мы можем говорить о том существует обширный мозговой субстрат для взаимодействия моторных и других систем мозга, включая память, эмоции и другие аспекты. Также были проведены исследования с использованием функциональной магнитно-резонансной томографии (фМРТ), которые показали активацию мозжечка во время выполнения когнитивных задач у испытуемых, не выполняющих двигательную активность (Bugalho, 2006).

Верхним конечностям принадлежит особая функциональная роль: в отличие от нижних они участвуют главным образом в выполнении точных произвольных движений. В выполнении произвольных движений задействованы все уровни нервной системы, и ведущую роль играет высший — кора головного мозга (Hauert, 1986; Iverson, 2010; Van der Fels и др.,2015).

Когнитивные навыки также связаны с задействованием высоких уровней контроля в мозге, в особенности коры (Friedman N. P.,2022). Это может быть одним из главных факторов, определяющих взаимосвязь развития когнитивных навыков и двигательных навыков (связанных с точными произвольными движениями). Когнитивные навыки и двигательные навыки развиваются одновременно и активно в возрасте от 5 до 10 лет (Anderson и др.,2001). В процессе моторного и когнитивного развития важное значение имеют психофизиологические процессы, такие как планирование последовательности действий и мониторинг (Roebers et al., 2009; Kojima, 2019). Эти процессы обеспечивают не только эффективное функционирование моторики, но и способствуют целенаправленного поведения. Интересно, что проблемы с мотивацией во время реабилитации одна из главных проблем (Blagovechtchenski, 2023).

Хотя описанные нейрофизиологические данные в некоторой степени подтверждают связь между моторным и когнитивным развитием у детей, тем не менее, в реальной клинике нет особых подходов к пациентам, связанных с особенностями когнитивного развития у детей с моторными нарушениями (Dusing S. C. и др., 2019).

С нашей точки зрения, оценка детей, с исследуемыми в данной работе, двигательными нарушениями часто ограничивается только их двигательной дисфункцией, оставляя без внимания их когнитивное развитие. Данное исследование было направлено на изучение особенностей развития когнитивных способностей детей с моторными нарушениями (множественным артрогрипозом и парезом Дюшена-Эрба).

В представленном исследовании мы сосредоточились на следующих проблемах:

1) Предыдущие исследования продемонстрировали возможную роль моторных функций детей в развитии когнитивных функций, но ни одно исследование не касалось особенностей такой взаимосвязи у детей с тяжелыми моторными заболеваниями верхних конечностей, такими как: множественный артрогрипоз (врожденное заболевание) и акушерским параличом плечевого сплетения («парез Дюшена-Эрба») (приобретенное заболевание). Оба заболевания имеют крайне схожую симптоматику и представляют модель для изучения связи развития моторных и когнитивных систем мозга, т.к. проявляются сразу при рождении ребенка и больше не прогрессируют (Агранович О. Е., и др., 2013).

2) Результаты исследований взаимосвязи моторных и когнитивных функций часто неоднозначны и противоречивы, поэтому требуется дополнительное методологическое исследование для определения оптимальных параметров измерений, позволяющих оценивать когнитивные функции не только при помощи психологических методик, но и методов психофизиологии, а также соотнесение этих методик между собой;

3) Не проводилось исследований электрофизиологической активности головного мозга детей с тяжелыми моторными заболеваниями (множественным артрогрипозом и парезом Дюшена-Эрба) с целью изучения различия данной группы детей от здоровой группы детей.

Раннее вмешательство, особенно направленное на развитие когнитивных функций, может предотвратить некоторые сопутствующие трудности в обучении и повседневной жизни детей с двигательными нарушениями (множественным артрогрипозом и парезом Дюшена-Эрба). В связи с этим текущее исследование было направлено на конкретизацию когнитивных проблем этих детей, для последующей адаптации программ абилитации.

1.2. Цели и задачи исследования

Цель - исследование взаимосвязи моторных и когнитивных функций у детей с нарушением развития верхних конечностей.

Задачи:

1) Исследование взаимосвязи моторных и когнитивных функций, выявление закономерностей когнитивной активности ребенка, связанной с развитием моторики;

2) Проведение исследования с помощью психологических метрик, сравнение уровня когнитивного развития детей с двигательными нарушениями верхних конечностей и здоровых детей; выявление взаимосвязи между моторным развитием и когнитивными функциями.

3) Проведение исследования с помощью ЭЭГ и анализ нейрональных коррелятов, лежащих в основе развития ребенка с моторными заболеванием, в сравнении со здоровыми детьми.

1.3. Методология и дизайн исследования

Описание пациентов

Для достижения поставленных целей в этом исследовании оценивались моторные функции детей с нарушениями движений верхних конечностей, такими как врожденный множественный артрогрипоз и парез Дюшена-Эрба (Копакта, 2021).

У детей с этими заболеваниями клинические характеристики, согласно ортопедической классификации, характеризуются общей патологией: контрактуры в двух и более крупных суставах, гипоплазия или аплазия мышц,

признаки нарушения работы мотонейронов в передних рогах спинного мозга (см. рис. 1).

Пациенты с данными заболеваниями верхних конечностей имеют определенный профиль - приводящая контрактура плечевого сустава, разгибательная (реже сгибательная) контрактура локтевого сустава, сгибательная контрактура лучезапястного сустава, сгибательные контрактуры пальцев, аддукторная контрактура большого пальца, гипоплазия или аплазия мышц верхних конечностей, ограничение или отсутствие самообслуживания (Корякина, 2021).

2) Мышцы верхних конечностей недоразвиты.

I

Рис.1. Пример пациента с диагнозом множественный артрогрипоз

В связи с этой общей патологией (контрактуры в суставах; гипоплазия или аплазия мышц; ограничения самообслуживания; признаки мотонейрональной

дисфункции) группа детей с артрогрипозом и группа детей с парезом Дюшена-Эрба были объединены в одну клиническую группу. А также не только с точки зрения симптоматики, но и с точки зрения лечения и абилитационных процессов, так как хирургические вмешательства и терапевтические процессы после них схожи при обоих заболеваниях. В клинической практике двигательные навыки восстанавливаются путем аутотрансплантации мышц из различных донорских зон.

У всех больных отмечено наличие симптомов, связанных с диагностированным заболеванием, другие нарушения (например, поражение головного мозга, нарушения слуха, зрения, родовые травмы) не были выявлены. Так же важно отметить, что исследования патологий при артрогрипозе показывают, что заболевание характеризуется именно поражением мотонейронов спинного мозга, при исключении остальных известных системных заболеваний (МКБ 10: Q74. 3. Приложение А. ГО: КР446).

Невролог оценивал моторное развитие по 4 компонентам (Перинатальное поражение ЦНС; Задержка моторного развития; Уровень пареза; Нарушение чувствительности) с помощью ренгенографии и осмотра. Невролог так же оценивал двигательную активность с помощью опросника АШЬНАМО, в котором родители отмечают способность ребенка выполнять бытовые действия по предложенной классификации А§гапоу1еЬ, ЬаЫпа (2013) (Агранович О.Е., 2013). Сумма данных оценок является общим баллом неврологического обследования.

Ортопед с помощью наблюдения за пациентом (например по углу сгибания-разгибания конечности) оценивал степень поражения конечностей, функциональные возможности пациента, виды схвата кисти, состояние мышц

проксимального отдела в/к, состояние мышц дистального отдела в/к, контрактуры в плечевом суставе, контрактуры в локтевом суставе, контрактуры в лучезапястном суставе, контрактуры пальцев кисти (Агранович О.Е., 2013). Общая сумма баллов является общей ортопедической оценкой двигательной активности.

Так же проводилось электромиографическое исследование, с помощью которой оценивается функциональное состояние периферических нервов, спинномозговых корешков и мышц (чувствительность, амплитуда, мышечные ответы).

Эффективность работы локтевого сустава у пациентов оценивалась с помощью модифицированной шкалы Ван Херста (Van Heest и др. 1998). Эта шкала включает оценку активного разгибания локтя, мышечной силы и развития навыков повседневной деятельности ребенка и использует адаптивные механизмы для сгибания локтя (толчок стола, упор туловища или шейное сгибание).

Запись и анализ ЭЭГ

В ходе исследования испытуемым/пациентам надевалась стандартная электродная шапочка по международной системе 10/10. ЭЭГ-активность регистрировалась при помощи 32 электродов с частотой дискретизации 500 Гц. Весь процесс обработки сигналов проводился с использованием программы MATLAB. При анализе ЭЭГ в первую очередь выделялись сегменты, соответствующие продолжительности каждого видеоблока, и временно выравнивались между испытуемыми и пациентами. Затем сигналы проходили высокочастотную фильтрацию (на частоте 1 Гц) и низкочастотную фильтрацию (на частоте 50 Гц). После выделения сегментов ЭЭГ, соответствующих длительности каждого стимула, электродные каналы с

высокой дисперсией идентифицировались вручную и заменялись на образцы с нулевым значением, что позволяло исключить их из последующего вычисления ковариационных матриц. Артефакты, связанные с движением глаз, удалялись с использованием алгоритма FastICA в среде MATLAB.

Оценка когнитивных функций

Для решения поставленных задач в данном исследовании оценивались когнитивные функции детей с двигательными нарушениями верхних конечностей, в частности, с артрогрипозом и парезом Дюшена-Эрба, а также контрольной группы здоровых детей. Группы детей с моторными нарушениями отбирались в Национальном медицинском исследовательском центре детской ортопедии и травматологии имени Г.И. Турнера.

Для оценки когнитивных функций детей, таких как концентрация внимания, слуховая память, зрительная память, наглядно-образное и логическое мышление и интеллект, использовался комплекс адаптированных диагностических методик так, чтобы он подходил максимальному количеству детей в имеющемся у нас возрастном диапазоне (3-15 лет).

Для оценки внимания и слуховой рабочей памяти использовался тест Векслера (Wechsler Intelligence Scale for Children, WISC-IV для детей от 6 лет, WPPSI для детей от 3-6 лет). Тест заключается в том, что ребенок повторяет ряд цифр за взрослым. Объём памяти исчисляется в количестве воспроизведенных цифр. Объём внимания исчисляется в количестве воспроизведенных цифр в обратном порядке.

Кратковременная зрительная рабочая память, наглядно-образное и логическое мышление, включающее процессы генерализации и способность выделять существенные признаки, измерялись с помощью методики из комплекса Шипициной "Психолого-педагогическая диагностика отклонений в развитии 16

детей младшего школьного возраста". Зрительная память измерялась в количестве запомненных и названных ребенком картинок, показанных ему. Мышление измерялось при помощи задания, которое включало в себя восстановление сюжета по картинкам. Испытуемому предъявлялось 6 карточек, в случайном порядке, ему было необходимо разложить карточки в правильном порядке и

Интеллект оценивался с помощью прогрессивных матриц Равена (А, В, С) (СРМ/СУБ и 8РМ+/МНУЗ). Ребенок выполнял задания, где должен был подобрать верную фигуру, которая вписывается в рисунок. Интеллект оценивался по шкале соответствия возрастному периоду, и переводился в стены [4].

1.4. Научная новизна

В данной работе впервые исследована связь когнитивных и моторных функций у больных множественным артрогрипозом и парезом Дюшена-Эрба. Впервые исследовано восприятие движения у больных множественным артрогрипозом и парезом Дюшена-Эрба. Исследованы различия восприятия и когнитивных функций в зависимости от степени поражения моторных функций.

Результаты данной работы вносят вклад в область теоретических моделей особенностей развития когнитивных функций и их взаимосвязи с моторными функциями, а именно, что двигательные нарушения (множественный артрогрипоз и парез Дюшена-Эрба) коррелируют с показателями внимания и памяти, и мы можем предполагать что вышеупомянутые моторные заболевания могут быть причиной когнитивной задержки, особенно в отношении зрительной и слуховой памяти.

Также наши результаты дополняют предыдущую работу по восприятию человеческого движения за счет внедрения натуралистических стимулов в экспериментальный план, и проведении данного исследования в группе детей с моторными нарушениями.

1.5. Методологическая новизна

Наше исследование вносит важный вклад в методологическую дискуссию о взаимосвязи моторных и когнитивных функций, и о влиянии моторной дисфункции верхних конечностей на когнитивное развитие детей. В частности, мы предоставили данные о различиях между детьми с задержкой моторного развития и здоровых детей, тем самым указав научному сообществу направление в причинно-следственном отношении данных факторов.

Кроме того, мы исследовали нейрональные корреляты восприятия движений здоровыми взрослыми и детьми, чтобы показать возрастные особенности восприятия видеостимулов, а затем провели аналогичное сравнение групп детей с моторными заболеваниями с контрольной группой здоровых детей.

Следует отметить, что наши исследования особенностей когнитивного развития детей с моторными заболеваниями верхних конечностей (множественным артрогрипозом и парезом Дюшена-Эрба) одни из первых в мире, однако, на наш взгляд, полученные нами результаты могут быть распространены и на другие моторные заболевания.

Эти результаты должны быть отражены в индивидуальных подходах к

обучению и абилитации детей с двигательными нарушениями

(множественным артрогрипозом и парезом Дюшена-Эрба). В то время как в

настоящее время широко используются специальные реабилитационные

программы, предназначенные для детей с различными нарушениями развития 18

(Decker и др. 2011), детям с двигательными нарушениями (множественным артрогрипозом и парезом Дюшена-Эрба) необходимы программы, специально адаптированные к их потребностям, учитывающие все нюансы их когнитивного развития, что отражено в настоящем исследовании. Такая программа была разработана нами для реализации в институте Турнера.

Улучшение двигательного развития у детей с множественным артрогрипозом и парезом Дюшена-Эрба, например, с помощью интерактивных видеоигр может стать новым направлением экспериментальных исследований. Разработанные игры могут быть эффективным инструментом для стимулирования медленного развития недостаточно развитых мышц у детей, что впоследствии может позволить оценить их влияние на когнитивное развитие. В перспективе такой подход поможет выяснить, какие конкретные аспекты необходимо учитывать при создании программ реабилитации и абилитации для детей с нарушениями движений.

1.6. Эмпирическая новизна

Мы впервые показали особенности различий между двумя группами детей, с моторными заболеваниями (множественным артрогрипозом и парезом Дюшена-Эрба) и здоровых детей. С помощью ЭЭГ мы показали особенности восприятия двигательной активности на видео с натуралистическими стимулами у здоровых взрослых, здоровых детей и детей с моторными нарушениями.

1.7. Положения, выносимые на защиту

1. Независимо от степени двигательной дисфункции у детей с моторными заболеваниями (множественным артрогрипозом и парезом Дюшена-Эрба) наблюдается задержка когнитивного развития (в особенности внимания и памяти). 19

2. Существуют значимые различия уровня когнитивного развития у детей с вышеупомянутыми моторными заболеваниями верхних конечностей и здоровых детей, особенно в возрастной период от 8-10 лет.

3. У детей с вышеупомянутыми моторными нарушениями и здоровых детей наблюдаются различные электрофизиологические нейрональные корреляты восприятия видео-стимулов, а именно, пациенты с врожденным множественным артрогрипозом или парезом Дюшена Эрба демонстрируют дивергентные нейрональные реакции на натуралистические видео.

1.8. Вклад автора

Автор принимал непосредственное участие в следующих этапах исследования: обзор соответствующей литературы, планирование и программирование экспериментальных парадигм, подбор батареи диагностических методов, анализ поведенческих данных, сбор данных для части исследования ЭЭГ, интерпретация и описание результатов.

2. ОПИСАНИЕ ИССЛЕДОВАНИЙ

В данной главе мы описываем основные тезисы методологии, дизайна, результатов и основных выводов исследований. В первой части (Исследование 1) мы сравнили когнитивное развитие детей с моторными заболеваниями (множественным артрогрипозом и парезом Дюшена-Эрба) внутри группы (в зависимости от диагноза).

Во второй части (Исследование 2) в дискуссии мы рассмотрели современное состояние исследований в области взаимосвязи моторных и когнитивных функций, а также сравнили когнитивное развитие детей с вышеупомянутыми моторными заболеваниями и контрольной группы здоровых детей.

В третьей части (Исследование 3) мы провели исследование с применением ЭЭГ для оценки особенностей нейрональных коррелятов, лежащих в основе восприятия движений человека на группе здоровых детей и взрослых. Кроме того, мы провели сравнение восприятия видео-стимулов группы здоровых детей с группой детей с вышеупомянутыми моторными заболеваниями.

2.1. Исследование 1. Исследование когнитивных особенностей детей с моторными нарушениями

В исследовании приняли участие три группы детей: пациенты с артрогрипозом, пациенты с парезом Дюшена-Эрба и здоровые дети. Было проведено сравнение когнитивного развития детей с разными моторными заболеваниями, и здоровых детей.

Внимание Слуховая память Зрительная память Интеллект Вербуя ьнп-логическое Н'эглядно-рбрэзное

^шпильЛророПарм Квиглоль Агпрв ПчХ! Контрил» Аргро П.1ри НомрмьАрфе П)р« КЬи1рйкь АрГро Пл»1 Кинраль Артцо Пари

Рис.2. Сравнение групп детей с артрогрипозом и парезом Дюшена-Эрба и здоровой группы детей по уровню развития когнитивных функций

Для этой задачи применялся тест Краскела-Уоллиса, для проверки гипотезы о том, что медианные показатели в различных когнитивных задачах равны среди испытуемых с артрогрипозом, пациентов с парезом Дюшена-Эрба и детей контрольной группы. Тест Манна-Уитни использовался в качестве апостериорного анализа для изучения точных различий между пациентами с артрогрипозом, пациентами с парезом Дюшена-Эрба и детьми из контрольной группы.

По уровню зрительной памяти, дети как в группе с артрогрипозом (и = 369,0, p = 0,023), так и в группе с парезом Дюшена-Эрба (и = 230,5, р = 0,046) значительно отличались от своих сверстников из контрольной группы, тогда как пациенты с артрогрипозом и с парезом Дюшена-Эрба показали одинаковые результаты в сравнении между собой (ц = 102,5, р = 1,00).

Аналогичный результат продемонстрировало сравнение уровня мышления, дети как в группе с артрогрипозом (ц = 353,5, p = 0,012), так и в группе с 22

парезом Дюшена-Эрба (и = 237,0, р = 0,004) значительно отличались от своих сверстников из контрольной группы, тогда как пациенты артрогрипозом и парезом Дюшена-Эрба показали равные результаты в сравнении между собой (и = 109,0, р = 1,00).

Также мы оценили разницу в двигательных навыках у детей с диагнозами артрогрипоз и парез Дюшена-Эрба. Серия тестов Манна-Уитни показала, что дети с парезом Дюшена-Эрба демонстрировали значительно более высокие двигательные способности, чем дети с артрогрипозом. В частности, они продемонстрировали высокие баллы по шкале задержка моторного развития (что означает меньшую задержку по данной шкале) (и = 24,4, р = 0,001), более высокие баллы общего моторного развития (и = 10,5, р <0,001) и более высокий уровень мышечной силы (уровень пареза) (и = 21,0, р <0,001) (Рис.2.).

Задержка моторного развития Общее моторное развитие Уровень пареза

** **« »♦»

артрогрипоз парез Дюшена-Эрба артрогрипоз парез Дюшена-Эрба артрогрип&з парез Дюшена-Эрба

Рис.3. Сравнение группы детей с артрогрипозом и парезом Дюшена-Эрба по параметрам моторного развития

Таким образом, несмотря на схожесть нарушений между пациентами, статистический анализ показал достоверную разницу в уровне двигательных

навыков у детей с диагнозом артрогрипоз и детей с диагнозом парез Дюшена-Эрба. Пациенты достоверно различались по всем двигательным показателям. По тестам на зрительную память и мышление дети с диагнозом отличались от здоровых детей. Наши данные подтверждают предположение о том, что нарушения двигательных функций связаны с нарушениями отдельных когнитивных функций. Это согласуется с данными, показывающими, что развитие двигательных навыков коррелирует с развитием когнитивных навыков (Н^аБЫоппа и др., 2017; 7еп§ и др., 2017).

2.2. Исследование 2. Исследования различий когнитивных функций детей с моторными заболеваниями и здоровых детей

В рамках данного исследования дети с моторными нарушениями верхних конечностей также были включены, однако они были распределены по трем возрастным группам: группа А (22 детей в возрасте 3-7 лет), группа В (24 детей в возрасте 8-10 лет) и группа С (11 детей в возрасте 11-15 лет) (Копакта, 2021). Группы были сформированы в соответствии с общепринятыми возрастными категориями в области развития психологии, а также согласно классификации Эльконина, которая учитывает три основных периода развития: дошкольный, младший школьный и средний школьный возраст.

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ПРИЛОЖЕНИЯ

ПРИЛОЖЕНИЕ А. Статья «Aberrant Auditory and Visual Memory Development of Children with Upper Limb Motor Disorders»

Koriakina, M.; Agranovich, O.; Petrova, E.; Kadieva, D.; Kopytin, G.; Ermolovich, E.; Moiseenko, O.; Alekseeva, M.; Bredikhin, D.; Bermudez-Margaretto, B.; et al. Aberrant Auditory and Visual Memory Development of Children with Upper Limb Motor Disorders. Brain Sci. 2021, 11, 1650. https:// doi.org/10.3390/brainsci11121650

Абстракт. Целью данного исследования было сравнить различия в когнитивном развитии детей с двигательными нарушениями верхних конечностей и без них. В исследовании приняли участие 89 детей в возрасте от 3 до 15 лет: 57 детей с аналогичными двигательными нарушениями верхних конечностей и 32 здоровых ребенка. Наши результаты показали, что двигательные нарушения могут ухудшать когнитивные функции, особенно память. В частности, мы обнаружили, что дети в возрасте от 8 до 11 лет с нарушениями верхних конечностей значительно отличаются от своих здоровых сверстников по шкалам слуховой и зрительной памяти. Корреляционный анализ не выявил значимой связи между другими когнитивными функциями (внимание, мышление, интеллект) и моторными функциями. В целом, полученные результаты указывают на необходимость адаптации общих программ абилитации для детей с двигательными нарушениями с учетом когнитивных нарушений в период их развития. Настоящее исследование показало важность когнитивных проблем для этих детей. Более того, раннее вмешательство, особенно направленное на развитие памяти, может предотвратить некоторые из сопутствующих трудностей в обучении и повседневной жизни детей с двигательными нарушениями.

brain sciences

Article

Aberrant Auditory and Visual Memory Development of Children with Upper Limb Motor Disorders

Maria Koriakina l,2,*/ Olga AgranovichEkaterina Petrova Dzerassa Kadieva 2, Grigory Kopytin 2, Evgenia Ermolovich Olesya Moiseenko 2 , Margarita Alekseeva 1/ Dimitri Bredikhin 2, Beatriz Bermudez-Margaretto 2 , Ioannis Ntoumanis 2, Anna N. Shestakova 2, Iiro P. Jaaskelainen 2,3 and Evgeny Blagovechtchenski1,2

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Citation: Koriakiria, M.; Agranovich, O.; Petrova, E.; Kadieva, D.; Kopytin, G.; Ermolovich, E.; Moiseenko, O.; Alekseeva, M.; Bredikhin, D.; Bermiidez-Margaretto, В.; et al. Aberrant Auditory find Visual Memory Development of Children with Upper Limb Motor Disorders. Brain Sci. 2021,11, 1650. https:// doi.org/103390/ brainsci 11121650

Academic Editor: Christian Collet

Received: 23 November 2021 Accepted: 10 December 2021 Published: 15 December 2021

Publisher's Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. [© ®

Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses /by / 4.0/).

1 Federal State Budgetary Institution the Turner Scientific Research Institute for Children's Orthopedics under the Ministry of Health of the Russian Federation, 196603 St. Petersburg, Russia; [e-mail] (O.A.); [e-mail] (E.P.); [e-mail] (E.E.); [e-mail] (M.A.); [e-mail] (E.B.)

2 Centre for Cognition and Decision Making, Department of Psychology, National Research University Higher School of Economics, 101000 Moscow, Russia; [e-mail] (D.K.); [e-mail] (G.K.); [e-mail] (O.M.); [e-mail] (D.B.); [e-mail] (B.B.-M.); [e-mail] (I.N.); [e-mail] (A.N.S.); [e-mail] (I.P.J.)

3 Brain and Mind Laboratory, Department of Neuroscience and Biomedical Engineering, School of Science, Aalto University, 02150 Espoo, Finland

* Correspondence: [e-mail]

Abstract: The current study aimed to compare differences in the cognitive development of children with and without upper limb motor disorders. The study involved 89 children from 3 to 15 years old; 57 children with similar upper limb motor disorders and 32 healthy children. Our results showed that motor disorders could impair cognitive functions, especially memory. In particular, we found that children between 8 and 11 years old with upper limb disorders differed significantly from their healthy peers in both auditory and visual memory scales. These results can be explained by the fact that the development of cognitive functions depends on the normal development of motor skills, and the developmental delay of motor skills affects cognitive functions. Correlation analysis did not reveal any significant relationship between other cognitive functions (attention, thinking, intelligence) and motor function. Altogether, these findings point to the need to adapt general habilitation programs for children with motor disorders, considering the cognitive impairment during their development. The evaluation of children with motor impairment is often limited to their motor dysfunction, leaving their cognitive development neglected. The current study showed the importance of cognitive issues for these children. Moreover, early intervention, particularly focused on memory, can prevent some of the accompanying difficulties in learning and daily life functioning of children with movement disorders.

Keywords: cognitive function; arthrogryposis; obstetrics palsy; children; motor disorder

1. Introduction

The relationship between cognitive and motor development has long been the focus of psychology and psychophysiology. Nonetheless, no consensus has been reached regarding the connection between motor and cognitive skills [1-4]. Moreover, the neural mechanisms underlying this link remain elusive. Studies have shown significant correlations between particular categories of motor and cognitive function, including complex motor skills and higher-order cognitive abilities. For example, Stockel and Hughes [5] showed a strong association between anticipatory motor planning and working memory. This motor-cognitive interaction during development was also shown in Abdelkarim's study [6], which reported that fostering children's physical fitness during primary school age could enhance

Brain Sci. 2021, 22,1650. https://doi.org/10.3390/brainscilll21650

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both motor and cognitive learning abilities related to academic achievement. However, the authors of one of the most recent reviews on this topic [1] report no significant correlation between motor and cognitive skills in 4 to 16-year-old healthy children. Other studies have revealed that middle school children show a stronger relationship between the main categories of motor and cognitive skills compared to older school children [1].

Importantly, the evidence for a strong connection between cognitive and motor development is not limited to the behavioral domain. Several neurobiological studies have shown co-activation among the cerebellum, basal ganglia, and prefrontal cortex during different motor and cognitive tasks, especially those that are complex, new, have changeable conditions, or require quick responses and concentration to be completed [7,8]. Furthermore, functional studies using fMRI showed the activation of the cerebellum during cognitive tasks in which no movement is involved [9]. A number of anatomical and functional imaging studies have shown that cerebellum function is affected in several cognitive and behavioral developmental disorders, such as attention deficit hyperactivity disorder, autism, and schizophrenia [7]. Importantly, this neurophysiological evidence corroborates the association between motor and cognitive development in children [10].

Thus, cognitive and motor development seem to be particularly interrelated. Indeed, motor and cognitive skills show a similar developmental timeline, especially between the ages of 5 and 10 years old [11], and share several main psychophysiological processes, such as sequencing, monitoring, and planning [12].

Considering the inconsistencies among previous findings, it is crucial to explicitly assess the connection between motor and cognitive development beyond correlational indices. In this sense, the study of clinical populations, in particular children with motor impairment, would significantly contribute to the understanding of the interplay between motor and cognitive function during development. Moreover, the establishment of a clear link between the development of motor and cognitive abilities as well as its underlying brain mechanisms would enable new and integrative rehabilitation approaches for the improvement of both cognitive and motor skills.

To address this question, this study assessed the cognitive function of children with upper limb motor disorders, in particular subjects with arthrogryposis multiplex congenita (AMC) and obstetric brachial plexus palsy (OBPL). Among motor-related diseases, AMC is known to be one of the most serious congenital malformations and is characterized by the presence of two or more major joint contractures, muscle aplasia or hypoplasia, and motoneuronal dysfunction in the anterior horns of the spinal cord. The lack of active movement in the joints of the upper extremities is one of the main problems causing the limitation or inability to self-care. In clinical practice, these motor skills are restored by autotransplantation of muscles from various donor areas. Rehabilitation after such operations is associated with, among other things, neuronal rearrangements in the central nervous system, both in the spinal cord and in the cerebral cortex [13]. OBPL is an injury to the brachial plexus that occurs during birth, usually as a result of a stretching injury from a difficult vaginal delivery. This results in paralysis of the upper limb, which is therefore non-congenital, unlike in the case of AMC [13].

Although the prognosis is generally considered to be good, 20-30% of individuals with OBPL have a residual deficit [14], severe OBPL can result in permanent impairment of arm function, skeletal malformation, cosmetic deformity, behavioral problems, and socioeconomic limitations [15,16]. Individuals with OBPL reportedly have defective motor programming [17]. For example, OBPL infants "forget their arm" during automatic movements [16], supporting the concept of impaired central motor programs in OBPL. Differences in automatic movements between the affected and unaffected sides are caused by incomplete central program development and may contribute to incomplete arm function recovery following OBPL [16]. To further contribute to the discussion of the intertwining of cognitive and motor development, we specifically assessed the state of different cognitive functions, such as attention/concentration, memory, and intelligence, in children with AMC and OBPL as compared with a control group of healthy children. The outcomes

2. Materials and Methods

2.1. Participants

A group of 57 children (27 girls) 3-15 years old (mean = 8.3) with upper limb motor disorders (35 subjects with AMC and 22 subjects with OBPL) were selected from the Turner National Medical Research Center for Children's Orthopedics and Trauma Surgery. A group of 32 healthy children (15 girls) 3-15 years old (mean = 9.6) with no history of visual, hearing, or cognitive disorders were selected as a control group (see Table SI in Supplementary Materials). Children in the control and motor-impaired groups received the same education according to state standards of general education, thus following the school curriculum for normally developing children.

Regarding their clinical characteristics, children with AMC and OPBL have the following common pathology as per orthopedic classification:

They have the presence of contractures in two or more large joints, hypoplasia or aplasia of muscles, and signs of problems with motoneurons in the anterior horns of the spinal cord. At the same time, the upper limb of a patient has a characteristic profile with the following characteristics: an adductor contracture in the shoulder joint, an extensor (less often, flexion) contracture in the elbow joint, a flexion contracture in the wrist joint, flexion contractures in the fingers, an adduction contracture of the thumb, hypoplasia or aplasia of the muscle of the upper limbs, and restriction or lack of self-service. The muscles of the upper limbs are hypoplastic or absent. Therefore, both AMC and OBPL were included in our research as the clinical group. All patients had symptoms associated with diagnosed diseases and other disorders (for example, brain damage) were not identified.

Children with upper motor disorders were then split into three groups according to their age: Group A (22 children, 3-7 years old), Group B (24 children, 8-10 years old), and Group C (11 children, 11-15 years old) (see Table S2 in Supplementary Materials). Groups were determined in accordance with the most generally accepted age subdivisions in developmental psychology and Elkonin's periodization, and in correspondence with the three main developmental periods—that is, preschool, primary school, and secondary school age. The same age subdivision was applied to children in the control group, resulting in Group A (6 children), Group B (13 children), and Group C (13 children).

2.2. Assessment of Cognitive Functions

A battery of diagnostic techniques was selected to assess children's cognitive functions of attention span, auditory memory, visual memory, conceptual development, and intelligence. Assessments were conducted individually with each child in a quiet room specially prepared for psychological testing. Two psychologists participated in the evaluation and interpretation of the results.

Attention and auditory working memory were assessed using the Wechsler Intelligence Scale for Children. The WISC-IV was used for children from six years and WPPSI was used for the 3-6-year age group [19,20]. Selected subtests consisted of the repetition of a set of numbers in forward and backward order. The child repeated after the experimenter a set of numbers, first in forward order, then in reverse order, with the opportunity to make one mistake. The total number of memorized digits was recorded on the form and

then converted into points, by which the level of attention and memory development was determined.

Attention is the behavioral and cognitive process of selective concentration on a discrete stimulus [21]. In this case, the attention is reflected in the child's ability to repeat backward the numbers he or she has heard.

Auditory working memory reflects an individual's ability to listen to information presented orally, encode it, immediately repeat it, and recall it after [21]. In this case, the number of digits the child has memorized reflects the volume of auditory working memory.

Short-term visual working memory was measured using Shipitsina's "Psychological diagnostics of deviations in the development of children of primary school age." [22]. Within the framework of this method, 10 pictures were presented one at a time (one picture per second), after which the participant was asked to recall and name the objects presented in the pictures. Visual working memory is a cognitive system that maintains a limited amount of visual information so that it can be quickly accessed to serve the needs of an ongoing task. The number of memorized pictures was recorded on the form and then translated into points, which determined the level of visual short-term memory.

Verbal logical thinking, an aspect of conceptual development that includes generalization processes and the ability to highlight essential features, was measured using the set of sequential pictures of Shipitsina's "Psychological diagnostics of deviations in the development of children of primary school age." [22]. After a randomly arranged set of pictures was displayed, children were required to put the pictures in order, making up a logical story. The complexity of the pictures was a function of the age of the participant: the higher the age, the greater the complexity. Thinking was assessed on a point scale, where important evaluation factors were the child's ability to identify cause-and-effect connections and ways of verbally conveying these connections (number of sentences, number of parts of speech used for this purpose, etc.).

These two tests from the set of Shipitsina were published by decision of the Scientific Council of the Institute of Special Pedagogy and Psychology at the R. Vollenberg International University for Family and Children.

The test for visual memory is very similar to the test VISMEM: Recovery Test (Tombaugh, T. N (1996). Test of memory retention: the TOMM. North Tonawanda, NY: Multi-Health Systems.) Furthermore, the test we have used is more appropriate for our age group.

The test for verbal logical thinking is similar to one of the sets of the Wechsler test (Wechsler, D. Wechsler Intelligence Scale for Children-IV Conceptual and Interpretive Guide. Indiana Univ.-Purdue Univ. Indianap. 2003.), but we did not take it exactly, again, because of the age range, which limited our choice of methods.

Finally, intelligence was evaluated using Raven's progressive matrices (A, B, C) [23]. We used two types of tests-CPM/CVS kit and SPM+/MHV, because of the age period of the children group. All children in group A are very close to four-year-old, therefore they were included into group A (older than three years and seven months). Participants were shown a series of pictures with progressive patterns and asked to choose the piece that logically fit the picture. Intelligence is the ability to think, learn from experience, solve problems, and adapt to new situations. The number of correct answers was converted to a point system adapted for each age period.

The tests containing this assessment battery were chosen partly based on the age range of the sample (from 3 to 15 years old) and in consideration of the time constraints for the diagnosis of each child (that is, 60 min, due to medical reasons). These methods thus allowed us to fully assess the main cognitive functions of motor-impaired and healthy children representing a wide range of ages.

General motor development (GMD) refers to a person's functional abilities, which were evaluated by a neurologist based on the ball system of self-care skills. The maximum number of points is 21. Subjects with a mild extent of functional impairment (level 3) scored 17-20 points on the self-care scale ovals. A moderate extent of severity (level 2)

corresponds to 9-16 points on the self-care scale, and a severe extent (level 1) corresponds to a self-care score of 8 or lower.

2.3. Statistical Analysis

All cognitive tests that were used to assess the performance of the participants provided balanced, non-skewed scores. Accordingly, we treated the participants' scores as interval data, which allowed us to evaluate the results by means of quantitative analysis. Specifically, the modulation of cognitive performance by the factors of group (either subjects with motor impairment or control children) and age (younger, medium, and older children) was tested by the means of a series of 2 x 3 univariate analyses of variance (ANOVA). To account for the family-wise error rate, the resulting p-values were corrected with respect to the false discovery rate (FDR) according to Benjamini and Hochberg [24], with a critical ¡/-value of 0.15.

Further, the link between GMD and performance in each cognitive task was evaluated by means of Kerndall's correlation coefficient (Kendall's tau), which is recommended by Khamis [24] for data sets of our type. Similar to the series of univariate ANOVAs, the revealed p-values were corrected with respect to the FDR according to Benjamini and Hochberg [25], with a critical (/-value of 0.15.

3. Results

The ANOVA showed that nearly all cognitive indices obtained across different tests were significantly affected by the age of the participants (see Table 1). In particular, older children were characterized by higher scores in attention, auditory and visual memory, storytelling, and average cognitive score (ACS) (see Table S3 in Supplementary Materials).

Table 1. Statistical results for cognitive performance (ANOVA) as a function of factors Group (df = 1; either patient or control), and Age (df = 2: either 3-7 years, 8-10 years, or 11-15 years).* p < 0.05, **p< 0.01, ***p< 0.001.

Attention Auditory Memory Visual Memory Intelligence Storytelling Thinking ACS

F (1,64) Group P « 1 F (2,64) Age P 1 F (2.64) Interaction P fi 1

2.64 0.11 0.04 0.15 15.63 < 0.001 *** 0.32 <0.001 0.72 0.49 0.02 0.57

11.72 < 0.01 ** 0.15 <0.01 15.01 < 0.001 *** 0.32 <0.001 0.94 0.4 0.03 0.56

15.59 < 0.001 »** 0.19 <0.001 11.07 <0.001*»* 0.25 <0.001 1.06 0.35 0.03 0.82

0.32 0.57 0 0.57 0.58 0.57 0.02 0.57 0.64 0.53 0.02 0.53

1.45 0.23 0.02 0.27 4.87 <0.05* 0.13 <0.05 1.75 0.18 0.05 1

16.55 < 0.001 *** 0.2 <0.001 1.34 0.27 0.04 0.31 1.09 0.34 0.03 1

18.51 < 0.001 **» 0.22 <0.001 22.19 < 0.001 *** 0.41 <0.001 1.02 0.37 0.03 0.64

Importantly, results revealed that scores obtained in both auditory and visual memory tests, the verbal-logical aspect of thinking, and the ACS were significantly different between the two groups (see Table S4 in Supplementary Materials). Specifically, across all these tests, the performance of subjects with motor impairments was significantly lower than that of the control group (see Figure 1 for the score distributions in auditory and visual memory tasks).

Further, we examined the interaction of GMD of the subjects and their performance in various cognitive tasks. As can be seen in Table 2, these analyses showed that auditory memory was significantly correlated with the GMD of children (rT = 0.26; p = 0.02, q = 0.13), as well as the attention span (rT = 0.24; p = 0.04, q = 0.11). Moreover, we also observed a relation between participant's visual memory and their GMD as a trend (rT = 0.20; p = 0.08; q = 0.16). Therefore, although we do technically reject the hypothesis regarding the correlation between participants' motor function and visual memory performance, we consider that a particular link between those variables might still be possible as a trend. Performances on the other tests were not significantly explained by GMD scores.

A separate analysis of different age groups allowed us to trace cognitive development in children with upper limb motor disorders and control children dynamically. As a result, we observed the delay of cognitive development in children with upper limb motor disorders on their memory performance in both visual and auditory domains. Specifically, the difference in memory performance between subjects with upper limb motor disorders and control children was most prominent in the range of 8-10 years, whereas older children caught up to their control peers.

It is noteworthy that in this age range, cognitive learning styles and personality are actively formed, which allows the child to form their own individual behavioral programs. Overall, this age is referred to as the period of active formation of voluntary regulation of behavior, reflection, and self-control [26]. Basically, children of this age are actively growing, and their brains are developing intensively. At a deeper level, subtler functional connections are being formed between different brain areas, which will ensure the complex work of the whole organism [27]. It has also been shown that children 8-10 years of age undergo the accelerated formation of those brain areas that are responsible for motor activity. Accordingly, their movements become more accurate and varied [28,29]. Our results show that these processes might not fully occur in children with motor development disorders at this age and essentially are shifted to an older age. Most importantly, our findings reveal that such motor impairment is likely responsible for the cognitive delay shown in these children, particularly with respect to visual and auditory memory.

Previous studies have shown that motor and cognitive development can be fundamentally attributed to ages 8-10 [12]. Moreover, contrary to the previously widespread belief that motor development begins and ends earlier than cognitive development, studies have shown that both motor and cognitive development have equally long and likely interconnected developmental schedules [29-31]. Considering the present findings, a particular connection between cognitive and motor development seems plausible. Specifically, impaired cognitive development (e.g., in the case of a mental disorder) is likely to lead to impaired motor development. However, in the case of children with upper limb motor disorders, an inverse relationship might be assumed: if motor development is delayed, the development of cognitive functions (especially memory) seems to be affected too. Studies suggest that some aspects of cognitive and motor control are highly correlated, especially in the age range of 8-10 years old [12,32]. The difference in memory performance between children with upper limb motor disorders and healthy children, as well as the significantly different VLT performance between these groups, also implies such a connection.

To reveal this motor-cognitive link in detail, we further attempted to explicitly analyze the association between motor development in children with upper limb motor disorders and their cognitive development assessed by means of a wide battery of tests. Importantly, we found a significant correlation between subjects' GMD and auditory memory performance. Moreover, we observed a correlation between the visual memory and the GMD at the level of the trend. However, we observed a correlation between the visual memory and the GMD at the level of the trend. Moreover, we suggest that the significant correlation between attention and general motor development might also be connected to the processes underlying decreased memory performance due to the strong link between attention and memory [33]. Of note, had we only focused on memory performance as the main aspect of cognitive development affected by impaired motor development, we would have found a significant connection between motor development and both modalities of memory. Accordingly, although we could not find a significant correlation between visual memory performance and cognitive development, a particular link between them might still persist. At the same time, our findings with regard to auditory memory are fully in line with previous studies showing the link between memory and motor skills [27,32,34]. We also suggest that GMD might be connected with other modalities of memory during a particular age range, and hence its effect could be blurred since the correlation analyses in the current study could not be performed separately for specific age ranges but rather were performed for the whole group of children. Future studies might attempt to clarify the link

between the motor development of children and their memory function in more detail; in this vein, we suggest using a larger sample size, which would allow us to conduct separate correlation analyses of different age groups.

We found no significant correlation between motor development and intelligence. The absence of such a relationship is in line with other studies confirming that motor and intellectual levels in healthy children are largely independent [35]. Likewise, no correlation was observed between motor development and attention, which is also in line with previous studies [30]. Moreover, VLT did not correlate with motor development in children with upper limb motor disorders, despite the fact that we observed a significant difference in VLT performance between this group and the control group. We suggest that the lack of such correlation might be because VLT is an indicator of a broad range of cognitive functions, not limited to memory. VLT begins to develop when more and more words are memorized, speech is embedded in children's activities, and they start to perform a planning function. Thus, VLT performance might be dependent on memory performance, but not determined by it, as it is also affected by other domains of cognitive functions.

Summing up, our results indicate that a connection between children's motor development and memory performance does exist, at least in the auditory domain. In order to account for a possible explanation for that phenomenon, developmental changes in both motor and cognitive function must be considered.

First, children participating in this study were experiencing a period of active improvement of motor skills, coordination, muscle control and reaction time, and facilitation of the coordination of the biggest muscles, which altogether leads to success in organized sports and games, improved coordination of small muscles, the mastery of complex own skills, and improved fine control [36]. Moreover, around the age of 8-10 years old, one might observe a noticeably smoother combination of motor actions and motor skills compared to younger children. Specifically, normal children can rotate, twirl and jump, and perform tasks that help them in sports [37,38]. In the cognitive sphere, this period is referred to as the concrete operational stage, a term proposed by the Swiss psychologist Jean Piaget. The concrete operational stage refers to the developmental period at which children begin to apply logic and goals to specific events [39]. It is also the time when an infant's brain undergoes a series of significant changes. Information passes through the nervous system at a faster rate, and different parts of the brain begin to work in concert with each other in new combinations [40].

We suggest that the delay in the cognitive development of children with upper limb motor disorders, particularly observed in memory performance, might occur because the simultaneous development of the aforementioned motor skills, which is necessary during the concrete operational stage, does not occur in children with upper limb motor disorders. Moreover, motor and cognitive functions might be connected on a deeper level, and hence may depend on the development of the same cortical and subcortical structures [41 ].

The interconnection of memory and motor development has also been observed in other studies, which have shown the effect of motor memory in action choice and in procedural learning. Thus, motor memory, considered an intrinsic property of the motor system, can impact not only motor behavior, depending on the constraints, but also higher cognitive functions [42]. Indeed, current theories on memory function consider that both declarative knowledge and procedural skills might be acquired based on sensorimotor interaction and interactive behavior [43^45].

Altogether, the assessment of cognitive skills in children with impaired motor abilities in the current study contributes to a better understanding of the complex interconnection between motor and cognitive development. Our analysis shows that memory seems to be the primary aspect of cognitive development affected by impaired motor function. For a more detailed understanding of such a link between memory and motor development, a more specific study is required [46].

Regarding the practical implications of this study, these results should be reflected in individualized educational and rehabilitation approaches for children with motor disorders.

Whereas special rehabilitation programs designed for children with different disabilities are widely used nowadays [47], children with motor impairments need programs specifically adapted to their needs, considering all the nuances of their cognitive development, as reflected in this study. The enhancement of motor development with, for example, the help of interactive video games may be a new avenue of experimental research. Along these lines, such games could be used to motivate children to slowly train their undeveloped muscles, and whether or not this influences their cognitive development could then be evaluated [48-50]. In the future, this approach could help to understand exactly what aspects are required to be considered during the development of rehabilitation and habilitation programs for motor-impaired children.

5. Conclusions

• Motor dysfunction of the upper limb does impair cognitive functions, especially auditory and visual memory.

• The link between cognitive skills and motor impairment is especially manifested between the ages of 8 and 10 years old.

• These findings must be considered in the development of rehabilitation programs for individuals with motor disorders.

Supplementary Materials: The following are available online at https://www.mdpi.com/article/10 .3390/brainscil 1121650/sl, Table SI: Average values by age of children with motor disorders and the control group, Table S2: Visual representation of the division into groups by age of children with motor disorders and the control group, Table S3: Means and standard deviation (SD) of scores for both groups of children in all age ranges, Table S4: Statistical results for cognitive performance (ANCOVA) as a function of factors Group (df = 1; either patient or control), Sex (df = 1; either male or female) and Age (continuous).

Author Contributions: Conceptualization, M.K. and O.A.; methodology, M.K., O.A., A.N.S. and E.B. formal analysis, B.B.-M., D.B. and I.N.; investigation, M.K., U.K., E.P., M.A., G.K., O.M., E.E. and E.B. data curation, B.B.-M., D.B. and I.N.; writing—original draft preparation, M.K., E.B., A.N.S. and I.P.J, visualization, D.B. and I.N.; supervision, M.K., O.A., E.B., A.N.S. and I.P.J.; project administration, M.K. and E.B.; funding acquisition, E.B., O.A., A.N.S. and I.P.J. All authors have read and agreed to the published version of the manuscript.

Funding: This research was funded by the Russian Science Foundation, (20-65-47016) and has been carried out using HSE unique equipment (Reg. num 354937).

Institutional Review Board Statement: The study was approved by the decision of the local ethics committee No. 19-3 dated 9 December 2019.

Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.

Data Availability Statement: The data presented in this study are available on request from the corresponding author. The data are not publicly available due to patient confidentiality.

Conflicts of Interest: The authors declare no conflict of interest.

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ПРИЛОЖЕНИЕ Б. Статья «Similar Cognitive Skill Impairment in Children with Upper Limb Motor Disorders Due to Arthrogryposis Multiplex Congenita and Obstetrical Brachial Plexus Palsy»

Blagovechtchenski, E.; Koriakina, M.; Bredikhin, D.; Agranovich, O.; Kadieva, D.; Ermolovich, E.; Jääskeläinen, I.P.; Shestakova, A.N. (2023) Similar Cognitive Skill Impairment in Children with Upper Limb Motor Disorders Due to Arthrogryposis Multiplex Congenita and Obstetrical Brachial Plexus Palsy. Int. J. Environ. Res. Public Health, 20, 1841. https://doi.org/10.3390/ ijerph20031841

Абстракт. Артрогрипоз (AMC) и акушерский паралич плечевого сплетения (OBPP) это двигательные расстройства со схожими симптомами (контрактуры и нарушение функции верхних конечностей). АМC это врожденное состояние, в то время как OBPP возникает в результате травмы во время родов. Несмотря на различия, эти заболевания идентичны по своим проявлениям и программам лечения. Мы сравнили когнитивные навыки детей с диагнозами AMC и OBPP со здоровыми детьми; мы также сравнили двигательные навыки детей с нарушениями и двигательные навыки детей с нарушениями, и здоровых детей. Пациенты в обеих группах значительно отличались от здоровых детей по таким психологическим параметрам, как "объем зрительной памяти" и "мышление". Кроме того, две группы детей с АМC и OBPP значительно отличались друг от друга по таким параметрам двигательных навыков, как "задержка моторного развития", "общее моторное развитие" и "уровень пареза". Двигательная функция верхних конечностей у детей с ОBPP была менее нарушена по сравнению с детьми с АМС Однако мы не обнаружили значительных различий в когнитивных нарушениях между детьми с АМC и детьми с ОBPP детьми. Это может свидетельствовать о том, что двигательные нарушения являются более значимыми для развития когнитивных нарушений.

International Journal of SES Environmental Research ggjyl and Public Health

Article

Similar Cognitive Skill Impairment in Children with Upper Limb Motor Disorders Due to Arthrogryposis Multiplex Congenita and Obstetrical Brachial Plexus Palsy

Evgeny Blagovechtchenski1,sf, Maria Koriakina 1/2, Dimitri Bredikhin Olga Agranovich 2, Dzerassa Kadieva Evgenia Ermolovich 2 , Iiro P. Jääskeläinen1,3 and Anna N. Shestakova 1

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Citation: Blagovechtchenski, E.; Koriakina, M; Bredikhin, D.; Agranovich, O.; Kadieva, D.; Ermolovich, E.; Jaaskelainen, IP.; Shestakova, AN. Similar Cognitive Skill Impairment in Children with Upper Limb Motor Disorders Due to Arthrogryposis Multiplex Congenita and Obstetrical Brachial Plexus Palsy. Int. J. Environ. Res. Public Health 2023, 20,1841. https: / /doi.org/10.3390/ ijerph20G3l841

Academic Editor: Paul B. Tchounwou

Received: 2 November 2022 Revised: 7 January 2023 Accepted: 12 January 2023 Published: 19 January 2023

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Copyright: © 2023 by the authois. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

1 Centre for Cognition & Decision Making, Institute for Cognitive Neurosceince, National Research University Higher School of Economics, 101000 Moscow, Russia

2 Federal State Budgetary Institution, The Turner Scientific Research Institute for Children's Orthopedics under the Ministry of Health of the Russian Federation, 196603 St. Petersburg, Russia

3 Brain and Mind Laboratory, Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, 00076 Espoo, Finland

* Correspondence: [e-mail]

Abstract: Arthrogryposis multiplex congenita (AMC) and obstetrical brachial plexus palsy (OBPP) are motor disorders with similar symptoms (contractures and the disturbance of upper limb function). Both conditions present as flaccid paresis but differ from each other in the pathogenesis: AMC is a congenital condition, while OBPP results from trauma during childbirth. Despite this difference, these diseases are identical in terms of their manifestations and treatment programmes. We compared the cognitive skills of children with AMC and OBPP diagnoses with those of healthy children; we also compared the motor skills of impaired children with those of healthy ones. The patients in both groups significantly differed from the healthy children with regard to psychological parameters, such as 'visual memory capacity' and 'thinking'. Moreover, the two groups with children with AMC and OBPP significantly differed from each other in motor skill parameters, such as 'delayed motor development', 'general motor development', and the 'level of paresis'. Upper limb motor function in the OBPP children was less impaired compared to that of the AMC children. However, we did not find any significant differences in cognitive deficits between the AMC children and the OBPP children. This may indicate that motor impairment is more significant than the underlying cause for the development of cognitive impairment; however, the factors causing this phenomenon require further study (e.g., social environment, treatment, and rehabilitation programme).

Keywords: cognitive function; arthrogryposis; obstetrics palsy; children; motor disorder

1. Introduction

Motor skills and cognitive skills are often discussed together in the context of human development. However, the extent to which one affects the other remains unclear. For example, the question of whether it is worth changing the educational programme for children with motor disabilities has not yet been resolved. In this study, we attempted to find a clearer answer to the following question: what is more important for the child—the diagnosis itself or its manifestation?

Motor development plays a critical role in children's understanding of the physical and social worlds [1]. However, the extent to which motor development affects cognitive skills remains unclear [2-4]. For example, the association between motor planning and working memory performance was shown [5]. In school-age children, a correlation has been found between physical activity and cognitive skills [6]. It can be hypothesised that special school programmes must be developed for children with motor deficits. However, in most countries, educational programmes for children with motor disorders are the same as those for healthy children.

Int. ]. Environ. Res. Public Health 2023, 20,1841. https://doi.org/10.3390/ijerph20031841

https://www.mdpi.com/joumal/ijerph

In this study, we focused on diseases associated with impaired functioning of the upper extremities. The upper limbs in humans have a special functional role: unlike the lower limbs, they are mainly involved in the performance of precise voluntary movements. In performing voluntary movements, all levels of the nervous system are involved, especially the highest—the cerebral cortex [7-9]. Cognitive skills are also associated with the involvement of higher levels of control in the brain. This may be the critical factor that determines the interaction between the level of development of cognitive skills and motor skills (associated with precise voluntary movements). Cognitive skills and motor skills exhibit a similar developmental timeline, especially between the ages of 5 and 10 years; they also share several important psychophysiological processes, such as sequencing, monitoring, and planning [10,11].

In this study, we assessed the cognitive skills and motor skills of children with upper limb movement disorders, specifically, congenital arthrogryposis multiplex (AMC) and obstetric brachial plexus palsy (OBPP). AMC refers to a group of congenital conditions characterised by joint contractures in two or more areas of the body. While the precise cause may be unknown for some individuals, the causes of AMC are variable and may include genetic, parental, and environmental factors as well as abnormalities that form during foetal development [12]. Individuals with AMC have limited joint movement, with or without muscle weakness, in the affected areas of the body. Contractures vary in distribution and severity and do not progress to previously unaffected joints, but they may change over time due to growth and treatment. The lack of active movement in the joints of the upper extremities is one of the main problems that limit or prevent self-care [13]. AMC is considered a congenital condition, and its pathology is not sufficiently clear. OBPP is an injury to the brachial plexus that occurs during childbirth, usually as a result of strain during a difficult vaginal delivery. This leads to the paralysis of the upper limb; thus, this condition is not congenital, unlike AMC [14]. A factor that was important to this study is that both diseases manifest in the same manner—similar dysfunctions of the upper limbs. Furthermore, surgical interventions and the therapy processes following such interventions are similar. In clinical practice, motor skills are restored through the autotransplantation of muscles from various donor areas [15]. Postoperative therapy involves therapeutic physiotherapy and special physical exercises. Notably, there is no difference between the recovery processes for either of these diseases [14]. Some cognitive skills in children have been shown to be associated with motor illnesses. Compared to healthy children, the capacity for visual and auditory memory is lower in patients with AMC or OBPP. This is particularly evident in children aged 8-11 years [16]. However, the extent to which the degree of movement impairment affects cognitive skills remains unclear.

In this study, we compared the cognitive skills of children with similar manifestations of upper limb motor dysfunction (including treatment and therapy methods) with the cognitive skills of healthy children of a similar age. The patients with OBPP initially had a higher level of motor skill development. We also compared how this difference in motor skills is reflected in the degree of development of cognitive skills. We also correlated the severity of the motor impairment with the level of cognitive performance.

2. Methods

2.1. Patients and Control Participants

This study had 28 control participants (16 males, 12 females; mean age ± std: 9.95 ± 3.38), 18 amyoplasia participants (10 males, 8 females; mean age ± std: 10.14 ± 2.40), and 11 OBPP participants (6 males, 5 females; mean age ± std: 10.64 ± 2.54).

2.2. Assessment of Cognitive Functions and Motor Functions

Cognitive functions (attention span, auditory memory, visual memory, conceptual development, and thinking) were measured using a battery of diagnostic techniques.

Attention and auditory memory were assessed using the Wechsler Intelligence Scale for Children (WISC). The WISC-IV was used for children over six years of age, and the

Wechsler Preschool and Primary Scale of Intelligence (WPPSI) was used for children aged 3-6 years [17]. Attention was reflected in a child's ability to repeat backward the numbers they had heard, and auditory working memory was reflected in the number of digits the child had memorised.

Intelligence was evaluated using Raven's progressive matrices (A, B, and C) [18]. We employed two types of tests, namely the CPM/CVS kit and SPM+/MHV, because of the age range of the children in the study. Intelligence was reflected in the number of correct responses to age-appropriate intellectual ability tasks.

Visual memory and conceptual development as an aspect of thinking were measured using Shipitsina's 'psychological diagnostics of deviations in the development of children of primary school age'. Visual working memory was reflected in the number of memorised pictures out of the 10 presented. Conceptual development was assessed by the number of points a child scored when composing a story from pictures.

Thinking was assessed using the 'exclusion of objects' technique. This technique is designed to study the features of thinking—first, the level of development and second, the qualitative characteristics of the generalisation process of visual materials [19].

During neurology examinations, the patient's general motor skills (GMD) were estimated. Anamnesis vitae included information about the patient in infancy. A developmental delay was indicated when a child had not reached particular milestones within the expected time period and his motor skills were different from those of a healthy child (DMD). We estimated passive and active movement in the joints, muscles strength, muscle volume, muscle tone, tendon reflexes, and sensation. The paresis level was estimated clinically by the scheme of segmental innervation of upper limb muscles. A lower level of paresis is associated with greater motor impairment in the patient, i.e., greater involvement of the distal muscles [15].

2.3. Statistical Anah/sis

The Kruskal-Wallis H test was used to test the hypothesis that population median performances in different cognitive tasks are equal among AMC patients, OBPP patients, and control children. Mann-Whitney tests were used to investigate the exact differences between AMC patients, OBPP patients, and control children.

3. Results

The patients were examined during their spare time. They attended the laboratory supervised either by their parents or medical personnel. Their self-care capabilities were significantly different from healthy children. The patients could not take food or perform hygiene actions (wash face and hands) on their own. Rather, they did so under the patronage of their parents or medical personnel. We also noticed that all the movements performed by the patients appeared to be slower compared to healthy children. We plan to quantify these skills. Visual communication did not differ between healthy children and patients.

Comparison of children with AMC, OBPP and healthy children based on the Kruskal-Wallis H-test showed that significant deviations were observed for such parameters as «Visual Memory» and «Thinking» (Table 1).

We also assessed the difference in motor skills between children with AMC and OBPP diagnoses (Figure 1). The series of Mann-Whitney tests revealed that OBPP children showed significantly higher motor performance than AMC children. Specifically, they demonstrated higher DMD scores (u = 24.4, p =0.001), higher GMD scores (u = 10.5, p < 0.001), and higher level of paresis (u = 21.0, p < 0.001).

and walking [30], among other impairments [1]. Therefore, on the one hand, it can be hypothesised that any motor impairment must directly lead to cognitive impairment. However, our data are partially inconsistent with this claim since they showed selectivity of cognitive impairment in motor diseases and did not show any differences in memory performance between AMC patients and OBPP, patients despite their prominent differences in the motor domain. In this situation, several factors can be identified that affect the impairment of cognitive skills. Cognitive skills are formed in relation to motor skills, and this relationship could be nonlinear. There may be a "ceiling" effect, when, in the case of restraining a specific motor function, the function of the world perception would be discretely violated and, accordingly, cognitive impairments have a similar severity [31-33]. Another important factor, in our opinion, would be the social environment, which is also important for the formation of the patient's cognitive skills. Although, there may be other reasons for the effects we discovered.

Among the various factors that may affect the complex link between the motor and cognitive domains of development, parenting appears to be of particular importance. The parents of children with motor disorders perform most basic activities, such as dressing, feeding, and washing, for their children from birth. Notably, as the child grows, no psychological separation from the parent occurs; they continue employing the same, albeit no longer age-matching, parenting approaches. It is difficult for parents to step back from such a role. They continue to perform actions for the child in the usual routine, thus inhibiting the child's physical development. Such a manifestation of overprotection in parents who have a child with a serious illness is common [34]. Several studies have shown that such parental behaviour inhibits both the cognitive and mental development of a child [35,36]. Furthermore, parental overprotection increases the level of anxiety in children, which also suppresses the development of cognitive functions [37,38]. Notably, in most countries, the treatment and rehabilitation of AMC patients and OBPP patients are not associated with the severity of disease manifestation. This may also result in the levelling of the factor of individuality.

The involvement of modern neurotechnology may facilitate an understanding of the psychophysiological changes that occur in the brain in children with motor disorders [39]. It has been shown that, in such children, there is a significant decrease in the power of the main EEG rhythms [40]; moreover, specific rearrangements in the brain that are associated with a change in the functional representation of certain muscles of the upper extremities have been found in children with AMC [41]. It is likely that similar changes should occur in children diagnosed with OBPP, but there is no exact data on this issue. Understanding the relationship between such significant reorganisations in the brain and the level of development of cognitive skills may make it possible to reconstruct the mechanisms of compensatory brain activity in children with motor disorders. This will enable the creation of neurotechnology that can help children with motor disorders. Regular clinical and neurophysiological estimation, an assessment of the needs in daily life, and knowledge of the social and family environments are key points for management.

Accordingly, to eliminate cognitive impairment in children with motor diseases, it is necessary to focus not only on the correction of motor dysfunctions but also on the minimisation of the effects of the children's social environment.

5. Conclusions

This study has yielded the following conclusions:

• Children with AMC and those with OBPP differ from healthy children in terms of

cognitive skills, such as visual memory and thinking.

• Children with AMC and those with OBPP differ in terms of motor skills but not in

cognitive tests.

• Presumably, the presence of a motor disease may be a more significant factor than its

degree of manifestation in explaining cognitive deficits.

Author Contributions: Conceptualization, E.B., M.K. and O.A.; methodology, M.K., OA., A.N.S. and E.B.; formal analysis, D.B. and I.P.J.; investigation, M.K, D.K., E.E. and E.B.; data curation, O.A., D.B. and M.K.; writing—original draft preparation, E.B., A.N.S. and I.P.J.; visualization, D.B.; funding acquisition, E.B., O.A., A.N.S. and I.P.J. All authors have read and agreed to the published version of the manuscript.

Funding: This research was funded by the Russian Science Foundation, (20-65-47016) and has been carried out using HSE unique equipment (Reg. num 354937).

Institutional Review Board Statement: The study was approved by the decision of the local ethics 243 committee No. 19-3 dated 9 December 2019.

Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.

Data Availability Statement: The data presented in this study are available on request from the corresponding author. The data are not publicly available due to patient confidentiality.

Conflicts of Interest: The authors declare no conflict of interest.

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ПРИЛОЖЕНИЕ В. Статья «Developmental differences in the perception of naturalistic human movements»

Ntoumanis I, Shestakova A, Koriakina M, Kadieva D, Kopytin G and Jaaskelainen IP (2023) Developmental differences in the perception of naturalistic human movements. Front. Hum. Neurosci. 16:1046277. doi: 10.3389/fnhum.2022.104627

Абстракт. Широко распространено мнение, что мы более внимательны к движущимся по сравнению со статичными стимулами. Однако нейронные корреляты, лежащие в основе восприятия человеческих движений, не были широко исследованы в экологически. Однако нейронные корреляты, лежащие в основе восприятия человеческих движений, не были широко исследованы в экологических условиях, равно как и аспект развития этого феномена. Здесь мы задались целью изучить, как движения человеческих конечностей, показанные в натуралистическом видео, влияют на вовлеченность внимания детей и молодых взрослых.

frontiers Frontiers in Human Neuroscience

type Original Research published 10 January 2023 do i 10.3389/fnhum.2022.1046277

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OPEN ACCESS

edited by

Ivana Konvalinka,

Technical University of Denmark,

Denmark

reviewed by

Jens Madsen,

City College of New York (CUNY). United States Irene Leo,

University of Padua, Italy

•correspondence

loannis Ntoumanis iannisntoumanis<ayahoo.com

specialty section

This article was submitted to Cognitive Neuroscience, a section of the journal Frontiers in Human Neuroscience

received 16 September 2022 accepted 19 December 2022 published 10 January 2023

citation

Ntoumanis I, Shestakova A. Koriakina M, Kadieva D, Kopytin Gand Jaaskelainen IP (2023) Developmental differences in the perception of naturalistic human movements. Front. Hum. Neurosci. 16:1046277. doi: 10.3389/fnhum.2022.1046277

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© 2023 Ntoumanis. Shestakova, Koriakina, Kadieva, Kopytin and Jaaskelainen. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use. distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

Developmental differences in the perception of naturalistic human movements

loannis Ntoumanis1*, Anna Shestakova1, Maria Koriakina12, Dzerassa Kadieva1, Grigory Kopytin1 and liro P. Jaaskelainen13

'international Laboratory of Social Neurobiology, Institute for Cognitive Neuroscience. HSE University. Moscow. Russia, federal State Budgetary Institution the Turner Scientific Research Institute for Children's Orthopedics Under the Ministry of Health of the Russian Federation. Saint-Petersburg, Russia, 'Brain and Mind Laboratory, Department of Neuroscience and Biomedical Engineering, Aalto University School of Science. Espoo. Finland

Introduction: It is widely believed that we are more attentive towards moving versus static stimuli. However, the neural correlates underlying the perception of human movements have not been extensively investigated in ecologically valid settings, nor has the developmental aspect of this phenomenon. Here, we set forth to investigate how human limb movements displayed in naturalistic videos influence the attentional engagement of children and young adults.

Methods: Thirty-nine healthy participants (4-26 years old) were presented with naturalistic videos featuring human goal-directed movements, while neural activity was recorded using electroencephalography (EEG). Video scenes were automatically annotated as containing arm, leg or no movement, using a machine learning algorithm. The viewers' attentional engagement was quantified by the intersubject correlation of EEG responses evoked by the videos.

Results: Our results demonstrate that scenes featuring limb movements, especially simultaneous arm and leg movements, elicit higher attentional engagement than scenes with no limb movement. Interestingly, this effect was found to diminish with age.

Discussion: Overall, our findings extend previous work on the perception of human motion by implementing naturalistic stimuli in the experimental design and extend the list of factors influencing the viewer's engagement exerted by naturalistic videos.

1. Introduction

For more than a century, moving stimuli have been believed to attract our attention more than static stimuli (Pillsbury, 1908; Washburn and Putney, 1998). Stimulus movements "force attention on us; they take us by storm, and we can offer no resistance" (Titchener, 1915). This phenomenon has played a crucial role for the development of species, since one's ability to detect biological movements in ones surroundings can be a matter of life or death in such extreme situations as that of being close to a lurking predator in the jungle. Earlier research on biological motion perception has relied on point-light displays of biological motion (e.g., Carter and Pelphrey, 2006), which differ markedly from real-world movements, leaving our understanding ofhowthe perception of human motion develops incomplete. Here, we investigate the perception of human limb movements displayed in naturalistic videos, while accounting for the developmental aspect of this phenomenon.

The perception of biological motion is often considered an automatic function due to its significance for survival (Thompson and Parasuraman, 2012). For instance, despite their limited visual attention skills, newborns are able to discriminate between point-light displays of biological versus non-biological motion (Simion et al., 2008). However, there are factors that appear to influence the perception of human movements, such as attention, motor, and visual experience (Jacobs et al., 2004; Thompson and Parasuraman, 2012). A characteristic of human actions is that they are defined by certain features, such as arms and legs that move in a specific way (Thompson and Parasuraman, 2012). Tracking these features requires both bottom-up (e.g., detect motion based on luminance modulation) and top-down processing (e.g., attentional tracking; Lu and Sperling, 1995; Whitney, 2006).

Importantly, both bottom-up and top-down processing have been found to improve with age, partly due to the maturation of ventral and dorsal visual streams (Parrish et al., 2005; Ghanouni et al., 2015). This is believed to lie beneath the development of motion perception with aging (Allison et al., 2000; Blakemore, 2012; Ghanouni et al., 2015). There are additional functional changes that occur in the brain during development that may affect biological motion perception. For example, the superior temporal sulcus (STS), which is a brain region activated during the perception of biological motion (Allison et al., 2000; Grossman et al., 2000; Grezes et al., 2001; Frith, 2007; Blakemore, 2012), is considered to undergo protracted development during adolescence (Blakemore, 2012). The specificity of STS for biological motion perception has thereby been found to increase with age (Carter and Pelphrey, 2006). In general, adults are more sensitive to biological motion than young children (Bertenthal and Pinto, 1993; Pinto, 2006; Blake and Shitlrar, 2007). However, given that the above conclusions have been largely driven by studies implementing point-light displays of biological motion, it is important to

further investigate the developmental aspect of the perception of human movements in an ecologically valid setting.

Naturalistic videos mimic the real world while being diverse and dynamic (Nastase et al., 2019). On the one hand, such stimuli are considered interesting and engaging (Lehne et al., 2015; Bezdek et al., 2017) and on the other hand, they allow us to decipher the neural dynamics in close-to-real-life settings (Saarimaki, 2021). Neuroimaging data corresponding to naturalistic stimuli are usually not analyzed with explicit response models, since it is challenging to build predictors of specific events (Nastase et al., 2019; Jaaskelainen et al., 2021). Instead, model-free approaches are preferred, such as intersubject correlation (ISC) analysis (Hasson et al., 2004; Dmochowski et al., 2012). Earlier research suggests that electroencephalography (EEG) ISC covaries with the attentional state of the subjects, with attentionally engaging videos increasing the ISC of EEG responses (Dmochowski et al., 2012; Cohen and Parra, 2016; Ki et al., 2016). Interestingly, younger individuals have been found to exhibit higher ISC (Petroni et al., 2018).

In the present study, we used a machine-learning algorithm to detect video scenes featuring arm or leg human movement, and we further assessed how these features influence the ISC of EEG responses to the video stimuli. Given that moving stimuli have been associated with increased attention, we hypothesized that video scenes displaying limb movements elicit higher ISC than scenes displaying no limb movement. Furthermore, since sensitivity to biological motion has been found to increase with age, we hypothesized that ISC is susceptible to video limb movements in a pronounced way in older participants.

2. Materials and methods 2.1. Participants

Twenty-three healthy children (11 females, aged 4-16 years, mean age = 10.34) and 16 healthy adults (10 females, aged 18-26 years, mean age = 20.19) participated in the experiment. The under-aged participants were accompanied by their parents. Informed consent was obtained from all participants or their legal guardians. The study was approved by the Institutional Review Board of the local ethics committee. Overall, the experiment was carried out in accordance with the recommendations of the Declaration of Helsinki and its amendments.

2.2. Stimuli

Each participant was presented with 83 silent clips integrated into 4 video blocks of 4 min each. The order of the

blocks was randomized across participants, whereas the order of the clips within each block was fixed (clips were integrated in a single.mp4 file presented to the subjects). The mean duration of the dips was 16 s and there was no narrative structure across them. There was no gap between consecutive clips of the same video block, and participants received no instruction about whether they should re-center their gaze before each dip starts. The background color of the videos was black. Each video included scenes with human motor activity, such as a child engaged in sports, as well as scenes without motor activity (this condition included both scenes featuring immobile humans and scenes with no human content, such as universe footage; Supplementär)' Table 1). The video stimuli can be found in Supplementär)' Videos 1-4.

Notably, the videos were presented in a silent mode, because the participants were simultaneously presented with a non-attended auditory oddball stimuli, the results of which will be separately reported elsewhere. Although performing distracting tasks while watching videos has been found to diminish neural synchronization of the subjects (Cohen et aL, 2018), the motor-related visual information could be retrieved by the participants even under the potential distraction caused by the oddball task Notably, the oddball task was not consistent across videos or participants, eliminating the possibility that the oddball task has confounded the data presented in this article.

2.3. EEG data collection and preprocessing

Electroencephalography activity was recorded by means of 32 electrodes at a sampling frequency of 500 Hz for children. The adults' brain activity was recorded by simultaneous EEG and MEG recording, yet in the current study we only report the EEG data which contained the signals of 64 electrodes at a sampling frequency of 1,000 Hz (which was downsampled at 500 Hz). In order to not bias the ISC analysis, we analyzed only the recordings of the 32 electrodes the two groups had in common. Moreover, because scene transitions in the videos could causes increases in the ISC that are not related to stimulus movements, we removed the EEG data corresponding to the first 5 s of each short clip within each video block.

The EEG preprocessing pipeline followed previous studies (Dmochowski et al., 2012; Cohen and Parra, 2016). First, the EEG segments corresponding to the duration of each video block were extracted and temporally aligned across subjects. Then, the signals were high-pass filtered at 1 Hz and low-pass filtered at 50 Hz. Next, the channels whose average power exceeded the mean channel power by 4 SDs were identified and replaced with zero valued samples, so that these channels do not affect the calculation of the covariance matrices. Eye-movement related artifacts were removed by Independent Component Analysis (ICA), using the fastICA algorithm (Hyviirinen, 1999).

Outliers were replaced with zero, as well as the samples 40 ms around them (before and after). As outliers we classified the samples whose magnitude exceeded 3 SDs of the mean magnitude of their corresponding channel. Lastly, the time course of each channel and each subject was z-scored. Provided that children and adults were recorded with different EEG systems, we 2-scored the time courses in order to control for any between-groups confounding factors. This step is typical in fMRI ISC studies (Nastase et al., 2019).

2.4. Intersubject correlation analysis

The intersubject correlation was measured via a correlated component analysis. Parra et al. (2018) offer a detailed description of the method. First, the data from all participants were concatenated for each video. Based on the concatenated data, between-subject and within-subject covariance matrices were computed for each stimulus. These matrices were then averaged over the four video blocks, so that all stimuli correspond to the same projection vectors (Cohen and Parra, 2016). After the optimization of the correlated components, we calculated the ISC of each subject in a leave-one-out approach. This resulted in a single number per participant, reflecting the level at which this participant's neural activity was synchronized with the neural activity of all other participants. The reported ISC values correspond to the sum of the three most correlated components, following previous studies (Cohen and Parra, 2016; Iotzov et al., 2017; Cohen et al., 2018; Petroni et al., 2018), allowing us to measure the overall level of neural synchronization regardless of each component's anatomical origin. We also computed the ISC over sliding time windows, in order to assess the dynamics of ISC as a function of the motor-related content of short video scenes. To that end, the recordings were divided into 1.5 s sliding windows, with 1.2 s overlap (300 ms resolutuion). The ISC of each time window was then calculated based on the previously estimated projection vectors W (Dmochowski et al., 2012). Code for conducting correlated component analysis has been previously published by Parra Lab (https://www.parralab.org/isc/).

Previous EEG ISC studies calculated the time-resolved ISC in time windows of 5 s (e.g., Dmochowski et al., 2012; Poulsen et al., 2017), while a recent analysis showed that ISC can be reliably measured on a time-scale of 10 s (Madsen and Parra, 2022). However, multiple naturalistic movements are possible to be displayed consecutively within such a long period, making it difficult to determine which type of movement was dominant within each time window. On the contrary, 1.5 s is a reasonable period for capturing individual quick movements of the videos' actors (based on our data, the average duration of arm movements was 1.36 s and the average duration of leg movements was 9.20 s), while achieving a reliable neural synchrony estimation (here, 1.5 s correspond to 750 time samples).

2.5. Automatic annotation of movements

The detection of arm and leg movements in the video stimuli was achieved in two steps First, a machine learning algorithm was employed to detect the arms and legs in each video frame of our stimuli (OpenPose demo; Cao et al., 2018). This algorithm is robust to multiple scales and to multiple people displayed on screen. Second, based on the Euclidean distance of each limb's screen coordinates between consecutive video frames, we detected the frames containing arm or leg movement The Euclidean distance had to be between two thresholds, so that we interpret that a movement occurred. The lower threshold served to filter out small, non-significant movement, like when the camera was not totally stable. The upper threshold served to filter out scene transitions. The optimal thresholds were selected by visually inspecting the output, since there is no ground truth in terms of when a movement occurred. This procedure resulted in a time series of motion indicators, which was then temporally aligned with the time-resolved ISC. That is to say, we determined during which time windows an arm or a leg movement was displayed. This analysis also excluded the first 5 s of each short clip within each video block, so that it is aligned with the ISC analysis. In general, employing a machine learning algorithm to track movements of human limbs has been found to be promising in studies of naturalistic human movements (Peterson etal., 2021). For the automatic annotation of movements, we implemented the OpenPose github repository (https://github.com/CMU-Perceptual-Computing-Lab/openpose), as in Ntoumanis et al. (2022).

2.6. Average luminance difference

A comparison of the ISC between scenes with human movements and scenes without human movements might be confounded by the fact that the former may contain higher level of visual dynamics, in general, compared to the latter. Therefore, we quantified the visual dynamics of the videos, using the Average luminance difference (ALD) across time, in order to examine the effect of human movements on ISC, after controlling for the overall visual dynamics. The ALD was calculated as in Poulsen et al. (2017). Specifically, the four videos were first converted to gray scale (0-255) by averaging over the RGB color channels. Then, we calculated the squared difference in pixel intensity between consecutive frames and calculated the average across pixels. The obtained ALD time series was then downsampled to match the temporal resolution of the ISC. The downsampling was done based on the maximum ALD per time window (Poulsen et al., 2017). This analysis also excluded the first 5 s of each short clip within each video block, so that it is aligned with the ISC analysis. Supplementary Figure 1

illustrates the correlation between ALD and ISC per component. Supplementary Figure 2 shows that there was no difference in ALD between scenes with different motor-related content.

2.7. Statistical analysis

After obtaining the time-resolved ISC and the time-resolved motion indicators, we estimated a linear mixed-effects model, with subject-level random effects (Bates et al., 2015), in order to predict ISC. Scenes with neither arm nor leg movement served as the reference level of the motor-related content of the stimulus and the occurrence of arm or leg (or both) movements were included as regressors. The model also assessed whether or not participants' age moderates the relationship between ISC and human movements displayed in the naturalistic videos. Finally, the ALD was also included in the model as a covariate, so that the effect of naturalistic movements on ISC is examined without the confound of general visual dynamics. A mixed-effects model was preferred over a typical fixed-effects one, because ISC has been found to significantly vary across individuals (Iotzov et al., 2017). Figure 1 illustrates the overall data analysis procedure.

3. Results

First, we estimated the components of the EEG signals that capture maximally correlated responses across subjects (Figure 1B). These component topographies were found similar to previous studies (Dmochowski et al., 2012,2014; Cohen and Parra, 2016; Iotzov et al., 2017; Cohen et al., 2018; Petroni et al., 2018). For instance, the first two components revealed a strong positivity at occipital sites, which is consistent with visual processing (Figure IB). This suggests that the highest ISC during video watching was achieved by similar processing of the visual stimuli. Overall, based on the scalp topographies the estimated correlated components were moderately perceptual and cognitive and not predominantly motor (Figure 1B).

A linear mixed-effects model with subject-level random effects was estimated in order to predict ISC based on the displayed human movements and participants' age, while accounting for visual dynamics. The results are summarized in Table 1. First of all, children exhibited significantly higher ISC compared to adults (p = 0.009), consistently with previous studies (Petroni et al., 2018). Also, the ISC was found to significantly increase with ALD (p < 0.0001), which is a measure of visual dynamics. This finding is also in line with earlier research (Poulsen et al., 2017). Moreover, displayed arm movements and leg movements were found to increase the ISC (p < 0.0001 and p = 0.003, respectively), especially when presented simultaneously (p < 0.0001). Importandy, participants' age significantly moderated the effect of simultaneous arm and leg movements on ISC (p < 0.0001).

A EEG recording during the stimulus

B Estimation of Hie coireUted components C resolved ISC

C2 C3

Oiiginal video stimulus

E Detection of »m-and leg-related movements F Time resolved

Linear mixed-effects model

Schematic representation of the data analysis. Based on the preprocessed electroencephalography (EEG) signals (A), we extracted components that are maximally correlated among participants (B) Using these components, we projected the EEG data to the so-called components' space and measured the intersubject correlation (ISC). We did this in a time-resolved fashion, i.e., repetitively for sliding time windows of 1.5 s size and 80% overlap. This revealed how the ISC changed across time (C) Furthermore, we applied a machine-learning algorithm to the original video stimulus (D) in order to detect scenes in the videos where arm- or leg-related movements occur (E). We did this in a time-resolved fashion, i.e., repetitively for sliding time windows of 1.5 s size and 80% overlap (F) Therefore, the time series displayed on panels (C,F) were perfectly temporarily aligned. Then, we estimated a linear mixed-effects model to predict the ISC based on the time-resolved movement indicators, while participants' age was included as a covariate.