Periventricular nodular heterotopia is coupled with the neocortex during resting and task states

Author:

Gao Yayue1,Chen Guanpeng234,Teng Pengfei5,Zhang Xin6,Fang Fang234,Englot Dario J7,Luan Guoming589,Wang Xiongfei58,Wang Qian2310

Affiliation:

1. Department of Psychology , Beihang University, Beijing 100191 , China

2. School of Psychological and Cognitive Sciences and Beijing Key Laboratory of Behavior and Mental Health , Peking University, Beijing 100871 , China

3. IDG/McGovern Institute for Brain Research , Peking University, Beijing 100871 , China

4. Peking-Tsinghua Center for Life Sciences , Peking University, Beijing 100871 , China

5. Department of Neurosurgery , Sanbo Brain Hospital, Capital Medical University, Beijing 100093 , China

6. Department of Neurology , The Children’s Hospital, Zhejiang University School of Medicine, National Clinical Research Center for Child Health, Hangzhou 310003 , China

7. Department of Neurological Surgery , Vanderbilt University Medical Center, Nashville, TN 37212 , USA

8. Beijing Key Laboratory of Epilepsy , Epilepsy Center, Sanbo Brain Hospital, Capital Medical University, Beijing 100093 , China

9. Beijing Institute for Brain Disorders , Beijing 100069 , China

10. Key Laboratory of Brain , Cognition and Education Sciences, Ministry of Education, South China Normal University, Guangzhou 510631 , China

Abstract

Abstract Periventricular nodular heterotopia (PVNH) is a well-defined developmental disorder characterized by failed neuronal migration, which forms ectopic neuronal nodules along the ventricular walls. Previous studies mainly focus on clinical symptoms caused by the PVNH tissue, such as seizures. However, little is known about whether and how neurons in the PVNH tissue functionally communicate with neurons in the neocortex. To probe this, we applied magnetoencephalography (MEG) and stereo-electroencephalography (sEEG) recordings to patients with PVNH during resting and task states. By estimating frequency-resolved phase coupling strength of the source-reconstructed neural activities, we found that the PVNH tissue was spontaneously coupled with the neocortex in the α–β frequency range, which was consistent with the synchronization pattern within the neocortical network. Furthermore, the coupling strength between PVNH and sensory areas effectively modulated the local neural activity in sensory areas. In both MEG and sEEG visual experiments, the PVNH tissue exhibited visual-evoked responses, with a similar pattern and latency as the ipsilateral visual cortex. These findings demonstrate that PVNH is functionally integrated into cognition-related cortical circuits, suggesting a co-development perspective of ectopic neurons after their migration failure.

Funder

Zhejiang Provincial Natural Science Foundation

Center for Advanced Study

National Natural Science Foundation of China

National Foundation for Science and Technology Development

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

Reference38 articles.

1. The role of periventricular nodular heterotopia in epileptogenesis;Aghakhani;Brain,2005

2. Intracranial electroencephalography reveals selective responses to cognitive stimuli in the periventricular heterotopias;Akkol;J Neurosci,2021

3. Functional MRI interactions between dysplastic nodules and overlying cortex in periventricular nodular heterotopia;Archer;Epilepsy Behav,2010

4. Long-range phase synchronization of high-frequency oscillations in human cortex;Arnulfo;Nat Commun,2020

5. Trekking across the brain: the journey of neuronal migration;Ayala;Cell,2007

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