Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex
The generation of purposive movement by mammals involves coordinated activity in the corticospinal and corticostriatal systems, which are involved in different aspects of motor control. In the motor cortex, corticospinal and corticostriatal neurons are closely intermingled, raising the question of w...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | en_US |
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Society for Neuroscience
2012
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| Online Access: | http://hdl.handle.net/1721.1/75315 |
| _version_ | 1826200237490831360 |
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| author | Kiritani, Taro Wickersham, Ian R. Seung, H. Sebastian Shepherd, Gordon M. G. |
| author2 | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences |
| author_facet | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Kiritani, Taro Wickersham, Ian R. Seung, H. Sebastian Shepherd, Gordon M. G. |
| author_sort | Kiritani, Taro |
| collection | MIT |
| description | The generation of purposive movement by mammals involves coordinated activity in the corticospinal and corticostriatal systems, which are involved in different aspects of motor control. In the motor cortex, corticospinal and corticostriatal neurons are closely intermingled, raising the question of whether and how information flows intracortically within and across these two channels. To explore this, we developed an optogenetic technique based on retrograde transfection of neurons with deletion-mutant rabies virus encoding channelrhodopsin-2, and used this in conjunction with retrograde anatomical labeling to stimulate and record from identified projection neurons in mouse motor cortex. We also used paired recordings to measure unitary connections. Both corticospinal and callosally projecting corticostriatal neurons in layer 5B formed within-class (recurrent) connections, with higher connection probability among corticostriatal than among corticospinal neurons. In contrast, across-class connectivity was extraordinarily asymmetric, essentially unidirectional from corticostriatal to corticospinal. Corticostriatal neurons in layer 5A and corticocortical neurons (callosal projection neurons similar to corticostriatal neurons) similarly received a paucity of corticospinal input. Connections involving presynaptic corticostriatal neurons had greater synaptic depression, and those involving postsynaptic corticospinal neurons had faster decaying EPSPs. Consequently, the three connections displayed a diversity of dynamic properties reflecting the different combinations of presynaptic and postsynaptic projection neurons. Collectively, these findings delineate a four-way specialized excitatory microcircuit formed by corticospinal and corticostriatal neurons. The “rectifying” corticostriatal-to-corticospinal connectivity implies a hierarchical organization and functional compartmentalization of corticospinal activity via unidirectional signaling from higher-order (corticostriatal) to lower-order (corticospinal) output neurons. |
| first_indexed | 2024-09-23T11:33:19Z |
| format | Article |
| id | mit-1721.1/75315 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T11:33:19Z |
| publishDate | 2012 |
| publisher | Society for Neuroscience |
| record_format | dspace |
| spelling | mit-1721.1/753152022-09-27T20:18:03Z Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex Kiritani, Taro Wickersham, Ian R. Seung, H. Sebastian Shepherd, Gordon M. G. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Massachusetts Institute of Technology. Media Laboratory Wickersham, Ian R. Seung, H. Sebastian The generation of purposive movement by mammals involves coordinated activity in the corticospinal and corticostriatal systems, which are involved in different aspects of motor control. In the motor cortex, corticospinal and corticostriatal neurons are closely intermingled, raising the question of whether and how information flows intracortically within and across these two channels. To explore this, we developed an optogenetic technique based on retrograde transfection of neurons with deletion-mutant rabies virus encoding channelrhodopsin-2, and used this in conjunction with retrograde anatomical labeling to stimulate and record from identified projection neurons in mouse motor cortex. We also used paired recordings to measure unitary connections. Both corticospinal and callosally projecting corticostriatal neurons in layer 5B formed within-class (recurrent) connections, with higher connection probability among corticostriatal than among corticospinal neurons. In contrast, across-class connectivity was extraordinarily asymmetric, essentially unidirectional from corticostriatal to corticospinal. Corticostriatal neurons in layer 5A and corticocortical neurons (callosal projection neurons similar to corticostriatal neurons) similarly received a paucity of corticospinal input. Connections involving presynaptic corticostriatal neurons had greater synaptic depression, and those involving postsynaptic corticospinal neurons had faster decaying EPSPs. Consequently, the three connections displayed a diversity of dynamic properties reflecting the different combinations of presynaptic and postsynaptic projection neurons. Collectively, these findings delineate a four-way specialized excitatory microcircuit formed by corticospinal and corticostriatal neurons. The “rectifying” corticostriatal-to-corticospinal connectivity implies a hierarchical organization and functional compartmentalization of corticospinal activity via unidirectional signaling from higher-order (corticostriatal) to lower-order (corticospinal) output neurons. 2012-12-10T17:05:41Z 2012-12-10T17:05:41Z 2012-04 2011-09 Article http://purl.org/eprint/type/JournalArticle 0270-6474 1529-2401 http://hdl.handle.net/1721.1/75315 Kiritani, T. et al. “Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal-Corticostriatal Microcircuit in Mouse Motor Cortex.” Journal of Neuroscience 32.14 (2012): 4992–5001. en_US http://dx.doi.org/10.1523/jneurosci.4759-11.2012 Journal of Neuroscience Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Society for Neuroscience SFN |
| spellingShingle | Kiritani, Taro Wickersham, Ian R. Seung, H. Sebastian Shepherd, Gordon M. G. Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex |
| title | Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex |
| title_full | Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex |
| title_fullStr | Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex |
| title_full_unstemmed | Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex |
| title_short | Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex |
| title_sort | hierarchical connectivity and connection specific dynamics in the corticospinal corticostriatal microcircuit in mouse motor cortex |
| url | http://hdl.handle.net/1721.1/75315 |
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