EEG Analysis of the Functional State of the Brain in 5- to 7-Year-Old Children
- 作者: Komkova Y.N.1, Sugrobova G.A2, Bezrukikh M.M.1
-
隶属关系:
- Institute of Developmental Physiology RAE
- Penza State University
- 期: 卷 109, 编号 7 (2023)
- 页面: 954-974
- 栏目: EXPERIMENTAL ARTICLES
- URL: https://medjrf.com/0869-8139/article/view/651551
- DOI: https://doi.org/10.31857/S0869813923070075
- EDN: https://elibrary.ru/XJCVZQ
- ID: 651551
如何引用文章
详细
The study is aimed at assessing individual and age-related features of the functional state of various parts of the brain and the patterns of their ontogenetic changes based on the structural analysis of resting-state electroencephalogram (EEG) patterns in 5- to 7-year-old children. The study involved 266 children, who were divided into different age groups: Group 1–5 years old (mean age 4.98 ± 0.33), Group 2–6 years old (mean age 6.03 ± 0.35), and Group 3–7 years old (mean age 6.85 ± 0.22). Alpha-rhythm parameters recorded mainly in the occipital areas may serve as an indicator for the functional maturation of the brain. Significant age-related changes in the alpha-rhythm parameters have been revealed. The presence of a regular alpha-rhythm with a frequency of 8 to 10 Hz increases from 5 to 7 years of age. The occurrence of the alpha-rhythm of reduced frequency significantly decreases by the age of 7 years, and the occurrence of the polyrhythmic alpha-rhythm – by the age of 6 years. These changes are caused both by complications of the structural and functional organization of the cerebral cortex at the cellular level, which occur throughout the studied age period, and the improvement of its relationships with subcortical structures. A decrease in the occurrence of high-amplitude alpha-range electrical activity (EA) with signs of hypersynchrony in the caudal regions may indicate the maturation of the system of nonspecific activation of the brainstem reticular formation from 5 to 7 years of age. Age dynamics is also manifested in a significant decrease in the EEG occurrence of theta-range EA, and its zonal distribution in 5- to 7-year-old children aged. Such changes specify the process of progressive formation of functional connections between individual areas of the cortex, as well as the cortex and subcortical structures, in particular thalamo-cortical ones. The occurrence of alpha-range EA (less than 5.0%) and beta-range EA (about 13.0%) arranged topographically in the anterior cortex did not differ significantly with age. However, generalized EEG activity in the form of different frequency range waves, which characterizes the functional state of predominantly hypothalamic structures, occurs reliably more often in 7-year-old children rather than in 5-year-old children. Such dynamics is presumably associated with an increased reactivity of the hypothalamic-pituitary system in response to adaptive stresses caused by the transition to systematic learning and can be considered as a distinctive feature of this age period. Due to great restructuring of the brain functioning, all its structures become especially sensitive to high intellectual and emotional stress, which is characteristic of preschool children nowadays. The novelty of this study is highlighted by the identification of patterns, structure and nature of EA changes in 5- to 7-year-old normotypical children’s brain to assess the functional state of the cortex and regulatory brain systems. The research results based on a large sample of children, growing up in modern social and cultural conditions, would provide guidance for the formation of age standards.
作者简介
Yu. Komkova
Institute of Developmental Physiology RAE
编辑信件的主要联系方式.
Email: julie.komkova@gmail.com
Russia, Moscow
G. Sugrobova
Penza State University
Email: julie.komkova@gmail.com
Russia, Penza
M. Bezrukikh
Institute of Developmental Physiology RAE
Email: julie.komkova@gmail.com
Russia, Moscow
参考
- Long X, Benischek A, Dewey D, Lebel C (2017) Age-related functional brain changes in young children. NeuroImage 155: 322–330. https://doi.org/10.1016/j.neuroimage.2017.04.059
- Steiner L, Federspiel A, Slavova N, Wiest R, Grunt S, Steinlin M, Everts R (2020) Functional topography of the thalamo-cortical system during development and its relation to cognition. Neuroimage 223: 117361. https://doi.org/10.1016/j.neuroimage.2020.117361
- Whedon M, Perry NB, Bell MA (2020) Relations between frontal EEG maturation and inhibitory control in preschool in the prediction of children’s early academic skills. Brain and Cognition 146: 105636. https://doi.org/10.1016/j.bandc.2020.105636
- Perone S, Palanisamy J, Carlson SM (2018) Age-related change in brain rhythms from early to middle childhood: Links to executive function. Dev Sci 21(6): e12691. https://doi.org/10.1111/desc.12691
- Machinskaya RI, Lukashevich IP, Fishman MN (1997) Dynamics of brain electrical activity in 5- to 8-year-old normal children and children with learning difficulties. Human Physiol 23(5): 517–522.
- Paulino C, Flores A, Gomez C (2011) Developmental Changes in the EEG Rhythms of Children and Young Adults Analyzed by Means of Correlational, Brain Topography and Principal Component Analysis. J Psychophysiol 25: 143–158. https://doi.org/10.1027/0269-8803/a000052
- Miskovic V, Ma X, Chou CA, Fan M, Owens M, Sayama H, Gibb BE (2015) Developmental changes in spontaneous electrocortical activity and network organization from early to late childhood. Neuroimage 118: 237–247. https://doi.org/10.1016/j.neuroimage.2015.06.013
- Cuevas K, Bell MA (2022) EEG frequency development across infancy and childhood. Gable PA, Miller MW, Bernat EM (eds). The Oxford handbook of human EEG frequency. Oxford. https://doi.org/10.1093/oxfordhb/9780192898340.013.13
- Feige B, Scheffler K, Esposito F, Di Salle F, Hennig J, Seifritz E (2005) Cortical and subcortical correlates of electroencephalographic alpha rhythm modulation. J Neurophysiol 93(5): 2864–2872. https://doi.org/10.1152/jn.00721.2004
- Eeg-Olofsson O (1970) The development of the electroencephalogram in normal children and adolescents from the age of 1 through 21 years. Acta Paediatr Scand Suppl 2 08:Suppl208: 1+.
- Cellier D, Riddle J, Petersen I, Hwang K (2021) The development of theta and alpha neural oscillations from ages 3 to 24 years. Dev Cogn Neurosci. 50: 100969. https://doi.org/10.1016/j.dcn.2021.100969
- Clarke AR, Barry RJ, McCarthy R, Selikowitz M (2001) Age and sex effects in the EEG: development of the normal child. Clin Neurophysiol 112(5): 806–814. https://doi.org/10.1016/s1388-2457(01)00488
- Marshall PJ, Bar-Haim Y, Fox NA (2002) Development of the EEG from 5 months to 4 years of age. Clin Neurophysiol 113(8): 1199–1208. https://doi.org/10.1016/s1388-2457(02)00163-3
- Kozhushko NY, Ponomarev VA, Matveev YK, Evdokimov SA (2011) Developmental features of the formation of the brain’s bioelectrical activity in children with remote consequences of a perinatal lesion of the CNS: II. EEG typology in health and mental disorders. Human Physiol 37(3): 271–277. https://doi.org/10.1134/S0362119711020095
- Ucles P, Lorente S, Rosa F (1996) Neurophysiological methods testing the psychoneural basis of attention deficit hyperactivity disorder. Childs Nerv Syst 12(4): 215–217. https://doi.org/10.1007/BF00301253
- Hofstee M, Huijding J, Cuevas K, Deković M (2022) Self-regulation and frontal EEG alpha activity during infancy and early childhood: A multilevel meta-analysis. Dev Sci 25(6): e13298. https://doi.org/10.1111/desc.13298
- Clarke AR, Barry RJ, Dupuy FE, McCarthy R, Selikowitz M, Johnstone SJ (2013) Excess beta activity in the EEG of children with attention-deficit/hyperactivity disorder: a disorder of arousal? Int J Psychophysiol 89(3): 314–319. https://doi.org/10.1016/j.ijpsycho.2013.04.009
- Lukashevich IP, Machinskaya RI, Fishman MN (1999) The EEG-expert automatic diagnostic system. Biomed Eng 33(6): 302–307.https://doi.org/10.1007/BF02385390
- Semenova OA, Machinskaya RI (2016) Assessing Regulatory Components of the Cognitive Performance in Children Aged 5-10 with EEG Patterns of the Limbic System Non-Optimal Functioning. Zh Vyssh Nerv Deiat Im I P Pavlova 66(4): 458–469. https://doi.org/10.7868/S0044467716040109
- Лукашевич ИП, Мачинская РИ, Шкловский ВМ (2004) Особенности вегетативной регуляции и характер судорог у детей с заиканием. Физиол человека 30(4): 50–53. [Lukashevich IP, Machinskaja RI., Shklovskij VM (2004) Features of autonomic regulation and the nature of seizures in children with stuttering. Human Physiol 30(4): 50–53. (In Russ)].
- Semenova OA, Machinskaya RI (2015) The influence of the functional state of brain regulatory systems on the efficiency of voluntary regulation of cognitive activity in children: ii. neuropsychological and eeg analysis of brain regulatory functions in 10–12-year-old children with learning difficulties. Human Physiol 41(5): 478–486. https://doi.org/10.1134/S0362119715050126
- Жирмунская ЕА (1991) Клиническая электроэнцефалография. Обзор литературы и перспективы использования метода. М. “МЭЙБИ”.[Zhirmunskaya EA (1991) Clinical Electroencephalography. Literature Review and Prospects for Using the Method M. “MEJBI”. (In Russ)].
- Goldman-Rakic PS, Porrino LJ (1985) The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol 242(4): 535–560. https://doi.org/10.1002/cne.902420406
- Seeber M, Cantonas LM, Hoevels M, Sesia T, Visser-Vandewalle V, Michel CM (2019) Subcortical electrophysiological activity is detectable with high-density EEG source imaging. Nat Commun 10(1): 753.https://doi.org/10.1038/s41467-019-08725-w
- Gatev P, Wichmann T (2009) Interactions between cortical rhythms and spiking activity of single basal ganglia neurons in the normal and parkinsonian state. Cereb Cortex 19(6): 1330–1344. https://doi.org/10.1093/cercor/bhn171
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57 (1): 289–300. https://doi.org/10.2307/2346101
- Bezrukikh MM, Loginova ES, Partsalis EM (2015) Children with impaired cognitive development: complex assessment and Intervention. Human Physiol 41(4): 356–366. https://doi.org/10.1134/S0362119715040040
- Hughes JR (1994) EEG in Clinical Practice. Second edition. Boston. Butterworth-Heinemann.
- Connemann BJ, Mann K, Lange-Asschenfeldt C, Ruchsow M, Schreckenberger M, Bartenstein P, Gründer G (2005) Anterior limbic alpha-like activity: a low-resolution electromagnetic tomography study with lorazepam challenge. Clin Neurophysiol 116(4): 886–894. https://doi.org/10.1016/j.clinph.2004.11.015
- Boldyreva GN (2018) Atypical forms of cerebral α-activity in the case of lesions in regulatory structures of the human brain. Human Physiol 44(3): 246–256. https://doi.org/10.1134/S0362119718020032
- Lozano-Soldevilla D (2018) On the physiological modulation and potential mechanisms underlying parieto-occipital alpha oscillations. Front Comput Neurosci 12: 23. https://doi.org/10.3389/fncom.2018.00023
- Remer J, Croteau-Chonka E, Dean DC, D’Arpino S, Dirks H, Whiley D, Deoni SCL (2017) Quantifying cortical development in typically developing toddlers and young children, 1–6 years of age. Neuroimage 153: 246–261. https://doi.org/10.1016/j.neuroimage.2017.04.010
- Цехмистренко ТА, Василева ВА, Шумейко НС, Черных НА (2009) Структурные преобразования коры больших большого мозга и мозжечка человека в постнатальном онтогенезе. В кн: Развитие мозга и формирование познавательной деятельности ребенка. Фарбер ДА, Безруких ММ (ред). М. Изд-во Московск психолого-социальн института. Воронеж “Модэк”. 9–63 [Cekhmistrenko TA, Vasileva VA, Humejko NS, Hernyh NA (2009) Structural changes of the human cerebral cortex and cerebellum in postnatal ontogenesis. In: Brain development and formation of cognitive activity. Farber DA, Bezrukih MM (red). M. Publ House of the Moscow Psychol and Social Institute. Voronezh “Modek”. 9–63. (In Russ)].
- Tsekhmistrenko TA, Chernykh NA (2013) Developmental Characteristics of The Microstructure of Layer V of the Frontal Cortex in Humans. Neurosci Behav Physiol 43: 582–586. https://doi.org/10.1007/s11055-013-9775-3
- Алферова ВВ (1990) Отражение возрастных особенностей функциональной организации мозга в электроэнцефалограмме покоя. В кн: Структурно-функциональная организация развивающегося мозга. Фарбер ДА, Семенова ЛК, Алферова ВВ (ред). Л. Наука. 45–65. [Alferova VV (1990) Reflection of age-related features of the functional organization of the brain in the resting electroencephalogram. In: Structural and functional organization of the developing brain. Farber DA, Semenova LK, Alferova VV (red). L. Nauka. 45–65. (In Russ)].
- Бетелева ТГ, Дубровинская НВ, Фарбер ДА (1977) Сенсорные механизмы развивающегося мозга. М. Наука. [Beteleva TG, Dubrovinskaya NV, Farber DA (1977) Sensory Mechanisms of the Developing Brain. M. Nauka (In Russ)].
- Латаш П (1968) Гипоталамус, приспособительная активность и электроэнцефалограмма. М. Наука [Latash P (1968) Hypothalamus, Adaptive Activity and Electroencephalogram. M. Nauka. (In Russ)].
- Фарбер ДА, Алферова ВВ (1972) Энцефалограмма детей и подростков. М. Педагогика [Farber DA, Alferova VV (1972) Electroencephalogram in Children and Adolescents. M. Pedagogika. (In Russ)].
- Ahmadi M, Kazemi K, Kuc K, Cybulska-Klosowicz A, Zakrzewska M, Racicka-Pawlukiewicz E, Helfroush MS, Aarabi A (2020) Cortical source analysis of resting state EEG data in children with attention deficit hyperactivity disorder. Clin Neurophysiol 131(9): 2115–2130. 10.1016/j.clinph.2020.05.028' target='_blank'>https://doi.org/doi: 10.1016/j.clinph.2020.05.028
- Бражник ЕС, Виноградова ОС, Каранов АМ (1984) Регуляция тета-активности септальных нейронов корковыми и стволовыми структурами. Журн высш нерв деятельн им ИП Павлова 34(1): 71–80. [Brazhnik ES, Vinogradova OS, Karanov AM (1984) Regulation of the theta activity of septal neurons by cortical and brain stem structures. Zh Vyssh Nerv Deiat Im IP Pavlova 34(1): 71–80. (In Russ)].
- Orekhova EV, Stroganova TA, Posikera IN, Elam M (2006) EEG theta rhythm in infants and preschool children. Clin Neurophysiol 117(5): 1047–1062. https://doi.org/ doi: 10.1016/j.clinph.2005.12.027
- Переслени ЛИ, Рожкова ЛА (1996) Нейрофизиологические механизмы нарушений прогностической деятельности у детей с трудностями обучения. Дефектология 5: 15–22. [Peresleni LI, Rozhkova LA (1996) Neurophysiological Mechanisms of Prognostic Disturbances in Children with Learning Difficulties. Defektologiya 5: 15–22. (In Russ)].
- Kim J, Woo J, Park YG, Chae S, Jo S, Choi JW, Jun HY, Yeom YI, Park SH, Kim KH, Shin HS, Kim D (2011) Thalamic T-type Ca(2)+ channels mediate frontal lobe dysfunctions caused by a hypoxia-like damage in the prefrontal cortex. J Neurosci 31(11): 4063–4073. https://doi.org/10.1523/JNEUROSCI.4493-10.2011
- Sarnthein J, Jeanmonod D (2007) High thalamocortical theta coherence in patients with Parkinson’s disease. J Neurosci 27(1): 124–131. https://doi.org/10.1523/JNEUROSCI.4493-10.2011
- Мельников МЕ (2021) Один феномен с множеством интерпретаций: асимметрия лобного альфа-ритма ЭЭГ у здоровых людей. Часть I. Успехи физиол наук 52(3): 56–80. [Melnikov ME (2021) A single phenomenon with a multitude of interpretations: eeg frontal alpha asymmetry in healthy people. Part I. Uspekhi fiziol nauk 52(3): 56–80. (In Russ)]. https://doi.org/10.31857/S0301179821030036
- Threadgill AH, Gable PA (2018) Resting beta activation and trait motivation: Neurophysiological markers of motivated motor-action preparation. Int J Psychophysiol 127: 46–51. https://doi.org/10.1016/j.ijpsycho.2018.03.002
- Kropotov JD (2016) Functional Neuromarkers for Psychiatry. Acad Press. https://doi.org/10.1016/C2012-0-07144-X
- Chiang CT, Ouyang CS, Yang RC, Wu RC, Lin LC (2020) Increased Temporal Lobe Beta Activity in Boys With Attention-Deficit Hyperactivity Disorder by LORETA Analysis. Front Behav Neurosci 14: 85. https://doi.org/10.3389/fnbeh.2020.00085
- Rozhkova LA (2008) EEG spectral power of young schoolchildren with perinatal pathology of the cns. Human Physiol 34(1): 22–32. https://doi.org/10.1007/s10747-008-1003-0
- Loo SK, Hale TS, Macion J, Hanada G, McGough JJ, McCracken JT, Smalley SL (2009) Cortical activity patterns in ADHD during arousal, activation and sustained attention. Neuropsychologia 47(10): 2114–2119. https://doi.org/10.1016/j.neuropsychologia
- Ogawa T, Sonoda H, Ishiwa S, Goto K, Kojou M, Sawaguchi H, Wakayama K, Suzuki M (1989) Developmental characteristics of the beta waves of EEG in normal healthy children. No To Hattatsu 21(5): 424–429.
- Biau E, Kotz SA (2018) Lower Beta: A Central Coordinator of Temporal Prediction in Multimodal Speech. Front Hum Neurosci 12: 434. https://doi.org/10.3389/fnhum.2018.00434
- Weiss S, Mueller HM (2012) “Too Many betas do not Spoil the Broth”: The Role of Beta Brain Oscillations in Language Processing. Front Psychol 3: 201. https://doi.org/10.3389/fpsyg.2012.00201
- Williams D, Tijssen M, Van Bruggen G, Bosch A, Insola A, Di Lazzaro V, Mazzone P, Oliviero A, Quartarone A, Speelman H, Brown P (2002) Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 125(Pt 7): 1558–1569. https://doi.org/10.1093/brain/awf156
- Lofredi R, Okudzhava L, Irmen F, Brücke C, Huebl J, Krauss JK, Schneider GH, Faust K, Neumann WJ, Kühn AA (2023) Subthalamic beta bursts correlate with dopamine-dependent motor symptoms in 106 Parkinson’s patients. NPJ Parkinsons Dis 9(1): 2. https://doi.org/10.1038/s41531-022-00443-3
- Iskhakova L, Rappel P, Deffains M, Fonar G, Marmor O, Paz R, Israel Z, Eitan R, Bergman H (2021) Modulation of dopamine tone induces frequency shifts in cortico-basal ganglia beta oscillations. Nat Commun 12(1): 7026. https://doi.org/10.1038/s41467-021-27375-5
- Sharott A, Magill PJ, Harnack D, Kupsch A, Meissner W, Brown P (2005) Dopamine depletion increases the power and coherence of beta-oscillations in the cerebral cortex and subthalamic nucleus of the awake rat. Eur J Neurosci 21(5): 1413–1422.https://doi.org/10.1111/j.1460-9568.2005.03973.x
补充文件
