Aberrant age-related alterations in spontaneous cortical activity in participants with cerebral palsy

IntroductionCerebral Palsy (CP) is the most common neurodevelopmental motor disability, resulting in life-long sensory, perception and motor impairments. Moreover, these impairments appear to drastically worsen as the population with CP transitions from adolescents to adulthood, although the underly...

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Main Authors: Hannah Bergwell, Michael P. Trevarrow, Elizabeth Heinrichs-Graham, Anna Reelfs, Lauren R. Ott, Samantha H. Penhale, Tony W. Wilson, Max J. Kurz
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2023.1163964/full
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author Hannah Bergwell
Michael P. Trevarrow
Elizabeth Heinrichs-Graham
Elizabeth Heinrichs-Graham
Anna Reelfs
Lauren R. Ott
Samantha H. Penhale
Tony W. Wilson
Tony W. Wilson
Max J. Kurz
Max J. Kurz
author_facet Hannah Bergwell
Michael P. Trevarrow
Elizabeth Heinrichs-Graham
Elizabeth Heinrichs-Graham
Anna Reelfs
Lauren R. Ott
Samantha H. Penhale
Tony W. Wilson
Tony W. Wilson
Max J. Kurz
Max J. Kurz
author_sort Hannah Bergwell
collection DOAJ
description IntroductionCerebral Palsy (CP) is the most common neurodevelopmental motor disability, resulting in life-long sensory, perception and motor impairments. Moreover, these impairments appear to drastically worsen as the population with CP transitions from adolescents to adulthood, although the underlying neurophysiological mechanisms remain poorly understood.MethodsWe began to address this knowledge gap by utilizing magnetoencephalographic (MEG) brain imaging to study how the amplitude of spontaneous cortical activity (i.e., resting state) is altered during this transition period in a cohort of 38 individuals with spastic diplegic CP (Age range = 9.80–47.50 years, 20 females) and 67 neurotypical controls (NT) (Age range = 9.08–49.40 years, Females = 27). MEG data from a five-minute eyes closed resting-state paradigm were source imaged, and the power within the delta (2–4 Hz), theta (5–7 Hz), alpha (8–12 Hz), beta (15–29 Hz), and gamma (30–59 Hz) frequency bands were computed.ResultsFor both groups, the delta and theta spontaneous power decreased in the bilateral temporoparietal and superior parietal regions with age, while alpha, beta, and gamma band spontaneous power increased in temporoparietal, frontoparietal and premotor regions with age. We also found a significant group x age interaction, such that participants with CP demonstrated significantly less age-related increases in the spontaneous beta activity in the bilateral sensorimotor cortices compared to NT controls.DiscussionOverall, these results demonstrate that the spontaneous neural activity in individuals with CP has an altered trajectory when transitioning from adolescents to adulthood. We suggest that these differences in spontaneous cortical activity may play a critical role in the aberrant motor actions seen in this patient group, and may provide a neurophysiological marker for assessing the effectiveness of current treatment strategies that are directed at improving the mobility and sensorimotor impairments seen in individuals with CP.
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spelling doaj.art-e989d30fded240a6b4916dd472ec40e22023-07-13T19:30:19ZengFrontiers Media S.A.Frontiers in Neurology1664-22952023-07-011410.3389/fneur.2023.11639641163964Aberrant age-related alterations in spontaneous cortical activity in participants with cerebral palsyHannah Bergwell0Michael P. Trevarrow1Elizabeth Heinrichs-Graham2Elizabeth Heinrichs-Graham3Anna Reelfs4Lauren R. Ott5Samantha H. Penhale6Tony W. Wilson7Tony W. Wilson8Max J. Kurz9Max J. Kurz10Institute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE, United StatesInstitute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE, United StatesInstitute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE, United StatesDepartment of Pharmacology & Neuroscience, Creighton University, Omaha, NE, United StatesInstitute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE, United StatesInstitute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE, United StatesInstitute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE, United StatesInstitute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE, United StatesDepartment of Pharmacology & Neuroscience, Creighton University, Omaha, NE, United StatesInstitute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE, United StatesDepartment of Pharmacology & Neuroscience, Creighton University, Omaha, NE, United StatesIntroductionCerebral Palsy (CP) is the most common neurodevelopmental motor disability, resulting in life-long sensory, perception and motor impairments. Moreover, these impairments appear to drastically worsen as the population with CP transitions from adolescents to adulthood, although the underlying neurophysiological mechanisms remain poorly understood.MethodsWe began to address this knowledge gap by utilizing magnetoencephalographic (MEG) brain imaging to study how the amplitude of spontaneous cortical activity (i.e., resting state) is altered during this transition period in a cohort of 38 individuals with spastic diplegic CP (Age range = 9.80–47.50 years, 20 females) and 67 neurotypical controls (NT) (Age range = 9.08–49.40 years, Females = 27). MEG data from a five-minute eyes closed resting-state paradigm were source imaged, and the power within the delta (2–4 Hz), theta (5–7 Hz), alpha (8–12 Hz), beta (15–29 Hz), and gamma (30–59 Hz) frequency bands were computed.ResultsFor both groups, the delta and theta spontaneous power decreased in the bilateral temporoparietal and superior parietal regions with age, while alpha, beta, and gamma band spontaneous power increased in temporoparietal, frontoparietal and premotor regions with age. We also found a significant group x age interaction, such that participants with CP demonstrated significantly less age-related increases in the spontaneous beta activity in the bilateral sensorimotor cortices compared to NT controls.DiscussionOverall, these results demonstrate that the spontaneous neural activity in individuals with CP has an altered trajectory when transitioning from adolescents to adulthood. We suggest that these differences in spontaneous cortical activity may play a critical role in the aberrant motor actions seen in this patient group, and may provide a neurophysiological marker for assessing the effectiveness of current treatment strategies that are directed at improving the mobility and sensorimotor impairments seen in individuals with CP.https://www.frontiersin.org/articles/10.3389/fneur.2023.1163964/fullmagnetoencephalographyresting statesensorimotorbetaneuroimaging
spellingShingle Hannah Bergwell
Michael P. Trevarrow
Elizabeth Heinrichs-Graham
Elizabeth Heinrichs-Graham
Anna Reelfs
Lauren R. Ott
Samantha H. Penhale
Tony W. Wilson
Tony W. Wilson
Max J. Kurz
Max J. Kurz
Aberrant age-related alterations in spontaneous cortical activity in participants with cerebral palsy
Frontiers in Neurology
magnetoencephalography
resting state
sensorimotor
beta
neuroimaging
title Aberrant age-related alterations in spontaneous cortical activity in participants with cerebral palsy
title_full Aberrant age-related alterations in spontaneous cortical activity in participants with cerebral palsy
title_fullStr Aberrant age-related alterations in spontaneous cortical activity in participants with cerebral palsy
title_full_unstemmed Aberrant age-related alterations in spontaneous cortical activity in participants with cerebral palsy
title_short Aberrant age-related alterations in spontaneous cortical activity in participants with cerebral palsy
title_sort aberrant age related alterations in spontaneous cortical activity in participants with cerebral palsy
topic magnetoencephalography
resting state
sensorimotor
beta
neuroimaging
url https://www.frontiersin.org/articles/10.3389/fneur.2023.1163964/full
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