Synaptic network structure shapes cortically evoked spatio-temporal responses of STN and GPe neurons in a computational model
IntroductionThe basal ganglia (BG) are involved in motor control and play an essential role in movement disorders such as hemiballismus, dystonia, and Parkinson's disease. Neurons in the motor part of the BG respond to passive movement or stimulation of different body parts and to stimulation o...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Neuroinformatics |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fninf.2023.1217786/full |
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| author | Justus A. Kromer Hemant Bokil Peter A. Tass |
| author_facet | Justus A. Kromer Hemant Bokil Peter A. Tass |
| author_sort | Justus A. Kromer |
| collection | DOAJ |
| description | IntroductionThe basal ganglia (BG) are involved in motor control and play an essential role in movement disorders such as hemiballismus, dystonia, and Parkinson's disease. Neurons in the motor part of the BG respond to passive movement or stimulation of different body parts and to stimulation of corresponding cortical regions. Experimental evidence suggests that the BG are organized somatotopically, i.e., specific areas of the body are associated with specific regions in the BG nuclei. Signals related to the same body part that propagate along different pathways converge onto the same BG neurons, leading to characteristic shapes of cortically evoked responses. This suggests the existence of functional channels that allow for the processing of different motor commands or information related to different body parts in parallel. Neurological disorders such as Parkinson's disease are associated with pathological activity in the BG and impaired synaptic connectivity, together with reorganization of somatotopic maps. One hypothesis is that motor symptoms are, at least partly, caused by an impairment of network structure perturbing the organization of functional channels.MethodsWe developed a computational model of the STN-GPe circuit, a central part of the BG. By removing individual synaptic connections, we analyzed the contribution of signals propagating along different pathways to cortically evoked responses. We studied how evoked responses are affected by systematic changes in the network structure. To quantify the BG's organization in the form of functional channels, we suggested a two-site stimulation protocol.ResultsOur model reproduced the cortically evoked responses of STN and GPe neurons and the contributions of different pathways suggested by experimental studies. Cortical stimulation evokes spatio-temporal response patterns that are linked to the underlying synaptic network structure. Our two-site stimulation protocol yielded an approximate functional channel width.Discussion/conclusionThe presented results provide insight into the organization of BG synaptic connectivity, which is important for the development of computational models. The synaptic network structure strongly affects the processing of cortical signals and may impact the generation of pathological rhythms. Our work may motivate further experiments to analyze the network structure of BG nuclei and their organization in functional channels. |
| first_indexed | 2024-03-12T13:59:29Z |
| format | Article |
| id | doaj.art-2a9c847358204a1aa49a93d4cd4915e7 |
| institution | Directory Open Access Journal |
| issn | 1662-5196 |
| language | English |
| last_indexed | 2024-03-12T13:59:29Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroinformatics |
| spelling | doaj.art-2a9c847358204a1aa49a93d4cd4915e72023-08-22T07:55:42ZengFrontiers Media S.A.Frontiers in Neuroinformatics1662-51962023-08-011710.3389/fninf.2023.12177861217786Synaptic network structure shapes cortically evoked spatio-temporal responses of STN and GPe neurons in a computational modelJustus A. Kromer0Hemant Bokil1Peter A. Tass2Department of Neurosurgery, Stanford University, Stanford, CA, United StatesBoston Scientific Neuromodulation, Valencia, CA, United StatesDepartment of Neurosurgery, Stanford University, Stanford, CA, United StatesIntroductionThe basal ganglia (BG) are involved in motor control and play an essential role in movement disorders such as hemiballismus, dystonia, and Parkinson's disease. Neurons in the motor part of the BG respond to passive movement or stimulation of different body parts and to stimulation of corresponding cortical regions. Experimental evidence suggests that the BG are organized somatotopically, i.e., specific areas of the body are associated with specific regions in the BG nuclei. Signals related to the same body part that propagate along different pathways converge onto the same BG neurons, leading to characteristic shapes of cortically evoked responses. This suggests the existence of functional channels that allow for the processing of different motor commands or information related to different body parts in parallel. Neurological disorders such as Parkinson's disease are associated with pathological activity in the BG and impaired synaptic connectivity, together with reorganization of somatotopic maps. One hypothesis is that motor symptoms are, at least partly, caused by an impairment of network structure perturbing the organization of functional channels.MethodsWe developed a computational model of the STN-GPe circuit, a central part of the BG. By removing individual synaptic connections, we analyzed the contribution of signals propagating along different pathways to cortically evoked responses. We studied how evoked responses are affected by systematic changes in the network structure. To quantify the BG's organization in the form of functional channels, we suggested a two-site stimulation protocol.ResultsOur model reproduced the cortically evoked responses of STN and GPe neurons and the contributions of different pathways suggested by experimental studies. Cortical stimulation evokes spatio-temporal response patterns that are linked to the underlying synaptic network structure. Our two-site stimulation protocol yielded an approximate functional channel width.Discussion/conclusionThe presented results provide insight into the organization of BG synaptic connectivity, which is important for the development of computational models. The synaptic network structure strongly affects the processing of cortical signals and may impact the generation of pathological rhythms. Our work may motivate further experiments to analyze the network structure of BG nuclei and their organization in functional channels.https://www.frontiersin.org/articles/10.3389/fninf.2023.1217786/fullbasal gangliaevoked responsesfunctional channelsnetwork connectivitymultichannel stimulationneural networks |
| spellingShingle | Justus A. Kromer Hemant Bokil Peter A. Tass Synaptic network structure shapes cortically evoked spatio-temporal responses of STN and GPe neurons in a computational model Frontiers in Neuroinformatics basal ganglia evoked responses functional channels network connectivity multichannel stimulation neural networks |
| title | Synaptic network structure shapes cortically evoked spatio-temporal responses of STN and GPe neurons in a computational model |
| title_full | Synaptic network structure shapes cortically evoked spatio-temporal responses of STN and GPe neurons in a computational model |
| title_fullStr | Synaptic network structure shapes cortically evoked spatio-temporal responses of STN and GPe neurons in a computational model |
| title_full_unstemmed | Synaptic network structure shapes cortically evoked spatio-temporal responses of STN and GPe neurons in a computational model |
| title_short | Synaptic network structure shapes cortically evoked spatio-temporal responses of STN and GPe neurons in a computational model |
| title_sort | synaptic network structure shapes cortically evoked spatio temporal responses of stn and gpe neurons in a computational model |
| topic | basal ganglia evoked responses functional channels network connectivity multichannel stimulation neural networks |
| url | https://www.frontiersin.org/articles/10.3389/fninf.2023.1217786/full |
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