Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy
Rolandic epilepsy (RE) is the most common focal, idiopathic, developmental epilepsy, characterized by a transient period of sleep-potentiated seizures and epileptiform discharges in the inferior Rolandic cortex during childhood. The cause of RE remains unknown but converging evidence has identified...
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| Format: | Article |
| Language: | English |
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Elsevier
2022-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S221315822200167X |
| _version_ | 1818219213176700928 |
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| author | Hunki Kwon Dhinakaran M. Chinappen Jonathan F. Huang Erin D. Berja Katherine G. Walsh Shi Wen Mark A. Kramer Catherine J. Chu |
| author_facet | Hunki Kwon Dhinakaran M. Chinappen Jonathan F. Huang Erin D. Berja Katherine G. Walsh Shi Wen Mark A. Kramer Catherine J. Chu |
| author_sort | Hunki Kwon |
| collection | DOAJ |
| description | Rolandic epilepsy (RE) is the most common focal, idiopathic, developmental epilepsy, characterized by a transient period of sleep-potentiated seizures and epileptiform discharges in the inferior Rolandic cortex during childhood. The cause of RE remains unknown but converging evidence has identified abnormalities in the Rolandic thalamocortical circuit. To better localize this transient disease, we evaluated Rolandic thalamocortical functional and structural connectivity in the sensory and motor circuits separately during the symptomatic and asymptomatic phases of this disease. We collected high resolution structural, diffusion, and resting state functional MRI data in a prospective cohort of children with active RE (n = 17), resolved RE (n = 21), and controls (n = 33). We then computed the functional and structural connectivity between the inferior Rolandic cortex and the ventrolateral (VL) nucleus of the thalamus (efferent pathway) and the ventroposterolateral (VPL) nucleus of the thalamus (afferent pathway) across development in children with active, resolved RE and controls. We compared connectivity with age in each group using linear mixed-effects models. We found that children with active RE have increasing thalamocortical functional connectivity between the VL thalamus and inferior motor cortex with age (p = 0.022) that is not observed in controls or resolved RE. In contrast, children with resolved RE have increasing thalamocortical structural connectivity between the VL nucleus and the inferior motor cortex with age (p = 0.025) that is not observed in controls or active RE. No relationships were identified between VPL nuclei and the inferior sensory cortex with age in any group. These findings localize the functional and structural thalamocortical circuit disruption in RE to the efferent thalamocortical motor pathway. Further work is required to determine how these circuit abnormalities contribute to the emergence and resolution of symptoms in this developmental disease. |
| first_indexed | 2024-12-12T07:36:05Z |
| format | Article |
| id | doaj.art-2a63c0409b1f4d8d8167c67603146489 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-12-12T07:36:05Z |
| publishDate | 2022-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-2a63c0409b1f4d8d8167c676031464892022-12-22T00:32:55ZengElsevierNeuroImage: Clinical2213-15822022-01-0135103102Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsyHunki Kwon0Dhinakaran M. Chinappen1Jonathan F. Huang2Erin D. Berja3Katherine G. Walsh4Shi Wen5Mark A. Kramer6Catherine J. Chu7Department of Neurology, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USADepartment of Neurology, Massachusetts General Hospital, Boston, MA, USA; Department of Mathematics and Statistics, Boston University, Boston, MA, USADepartment of Neurology, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USADepartment of Neurology, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USADepartment of Neurology, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USADepartment of Neurology, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USADepartment of Mathematics and Statistics, Boston University, Boston, MA, USA; Center for Systems Neuroscience, Boston University, Boston, MA, USADepartment of Neurology, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USA; Corresponding author at: 175 Cambridge St, Suite 340, Boston, MA 02140, USA.Rolandic epilepsy (RE) is the most common focal, idiopathic, developmental epilepsy, characterized by a transient period of sleep-potentiated seizures and epileptiform discharges in the inferior Rolandic cortex during childhood. The cause of RE remains unknown but converging evidence has identified abnormalities in the Rolandic thalamocortical circuit. To better localize this transient disease, we evaluated Rolandic thalamocortical functional and structural connectivity in the sensory and motor circuits separately during the symptomatic and asymptomatic phases of this disease. We collected high resolution structural, diffusion, and resting state functional MRI data in a prospective cohort of children with active RE (n = 17), resolved RE (n = 21), and controls (n = 33). We then computed the functional and structural connectivity between the inferior Rolandic cortex and the ventrolateral (VL) nucleus of the thalamus (efferent pathway) and the ventroposterolateral (VPL) nucleus of the thalamus (afferent pathway) across development in children with active, resolved RE and controls. We compared connectivity with age in each group using linear mixed-effects models. We found that children with active RE have increasing thalamocortical functional connectivity between the VL thalamus and inferior motor cortex with age (p = 0.022) that is not observed in controls or resolved RE. In contrast, children with resolved RE have increasing thalamocortical structural connectivity between the VL nucleus and the inferior motor cortex with age (p = 0.025) that is not observed in controls or active RE. No relationships were identified between VPL nuclei and the inferior sensory cortex with age in any group. These findings localize the functional and structural thalamocortical circuit disruption in RE to the efferent thalamocortical motor pathway. Further work is required to determine how these circuit abnormalities contribute to the emergence and resolution of symptoms in this developmental disease.http://www.sciencedirect.com/science/article/pii/S221315822200167XfMRIDTINetworkBECTSCECTSSeLECTS |
| spellingShingle | Hunki Kwon Dhinakaran M. Chinappen Jonathan F. Huang Erin D. Berja Katherine G. Walsh Shi Wen Mark A. Kramer Catherine J. Chu Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy NeuroImage: Clinical fMRI DTI Network BECTS CECTS SeLECTS |
| title | Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy |
| title_full | Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy |
| title_fullStr | Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy |
| title_full_unstemmed | Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy |
| title_short | Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy |
| title_sort | transient developmental functional and structural connectivity abnormalities in the thalamocortical motor network in rolandic epilepsy |
| topic | fMRI DTI Network BECTS CECTS SeLECTS |
| url | http://www.sciencedirect.com/science/article/pii/S221315822200167X |
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