Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations
In networks of excitatory and inhibitory neurons with mutual synaptic coupling, specific drive to sub-ensembles of cells often leads to gamma-frequency (25–100 Hz) oscillations. When the number of driven cells is too small, however, the synaptic interactions may not be strong or homogeneous enough t...
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| Format: | Article |
| Language: | en_US |
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Public Library of Science
2012
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| Online Access: | http://hdl.handle.net/1721.1/70468 https://orcid.org/0000-0001-7132-8706 |
| _version_ | 1826213474518171648 |
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| author | Borgers, Christoph LeBeau, Fiona E. N. Boyden, Edward Stuart Kopell, Nancy J. Franzesi, Giovanni Talei |
| author2 | Massachusetts Institute of Technology. Media Laboratory |
| author_facet | Massachusetts Institute of Technology. Media Laboratory Borgers, Christoph LeBeau, Fiona E. N. Boyden, Edward Stuart Kopell, Nancy J. Franzesi, Giovanni Talei |
| author_sort | Borgers, Christoph |
| collection | MIT |
| description | In networks of excitatory and inhibitory neurons with mutual synaptic coupling, specific drive to sub-ensembles of cells often leads to gamma-frequency (25–100 Hz) oscillations. When the number of driven cells is too small, however, the synaptic interactions may not be strong or homogeneous enough to support the mechanism underlying the rhythm. Using a combination of computational simulation and mathematical analysis, we study the breakdown of gamma rhythms as the driven ensembles become too small, or the synaptic interactions become too weak and heterogeneous. Heterogeneities in drives or synaptic strengths play an important role in the breakdown of the rhythms; nonetheless, we find that the analysis of homogeneous networks yields insight into the breakdown of rhythms in heterogeneous networks. In particular, if parameter values are such that in a homogeneous network, it takes several gamma cycles to converge to synchrony, then in a similar, but realistically heterogeneous network, synchrony breaks down altogether. This leads to the surprising conclusion that in a network with realistic heterogeneity, gamma rhythms based on the interaction of excitatory and inhibitory cell populations must arise either rapidly, or not at all. For given synaptic strengths and heterogeneities, there is a (soft) lower bound on the possible number of cells in an ensemble oscillating at gamma frequency, based simply on the requirement that synaptic interactions between the two cell populations be strong enough. This observation suggests explanations for recent experimental results concerning the modulation of gamma oscillations in macaque primary visual cortex by varying spatial stimulus size or attention level, and for our own experimental results, reported here, concerning the optogenetic modulation of gamma oscillations in kainate-activated hippocampal slices. We make specific predictions about the behavior of pyramidal cells and fast-spiking interneurons in these experiments. |
| first_indexed | 2024-09-23T15:49:47Z |
| format | Article |
| id | mit-1721.1/70468 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T15:49:47Z |
| publishDate | 2012 |
| publisher | Public Library of Science |
| record_format | dspace |
| spelling | mit-1721.1/704682022-09-29T16:24:57Z Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations Borgers, Christoph LeBeau, Fiona E. N. Boyden, Edward Stuart Kopell, Nancy J. Franzesi, Giovanni Talei Massachusetts Institute of Technology. Media Laboratory Boyden, Edward Franzesi, Giovanni Talei In networks of excitatory and inhibitory neurons with mutual synaptic coupling, specific drive to sub-ensembles of cells often leads to gamma-frequency (25–100 Hz) oscillations. When the number of driven cells is too small, however, the synaptic interactions may not be strong or homogeneous enough to support the mechanism underlying the rhythm. Using a combination of computational simulation and mathematical analysis, we study the breakdown of gamma rhythms as the driven ensembles become too small, or the synaptic interactions become too weak and heterogeneous. Heterogeneities in drives or synaptic strengths play an important role in the breakdown of the rhythms; nonetheless, we find that the analysis of homogeneous networks yields insight into the breakdown of rhythms in heterogeneous networks. In particular, if parameter values are such that in a homogeneous network, it takes several gamma cycles to converge to synchrony, then in a similar, but realistically heterogeneous network, synchrony breaks down altogether. This leads to the surprising conclusion that in a network with realistic heterogeneity, gamma rhythms based on the interaction of excitatory and inhibitory cell populations must arise either rapidly, or not at all. For given synaptic strengths and heterogeneities, there is a (soft) lower bound on the possible number of cells in an ensemble oscillating at gamma frequency, based simply on the requirement that synaptic interactions between the two cell populations be strong enough. This observation suggests explanations for recent experimental results concerning the modulation of gamma oscillations in macaque primary visual cortex by varying spatial stimulus size or attention level, and for our own experimental results, reported here, concerning the optogenetic modulation of gamma oscillations in kainate-activated hippocampal slices. We make specific predictions about the behavior of pyramidal cells and fast-spiking interneurons in these experiments. Collaborative Research in Computational Neuroscience National Institutes of Health (U.S.) (grant 1R01 NS067199) National Institutes of Health (U.S.) (grant DMS 0717670) National Institutes of Health (U.S.) (grant 1R01 DA029639) National Institutes of Health (U.S.) (grant 1RC1 MH088182) National Institutes of Health (U.S.) (grant DP2OD002002) Paul G. Allen Family Foundationn Google (Firm) 2012-04-27T21:05:58Z 2012-04-27T21:05:58Z 2012-02 2011-06 Article http://purl.org/eprint/type/JournalArticle 1553-734X 1553-7358 http://hdl.handle.net/1721.1/70468 Borgers, Christoph et al. “Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations.” Ed. Olaf Sporns. PLoS Computational Biology 8.2 (2012): e1002362. Web. 27 Apr. 2012. https://orcid.org/0000-0001-7132-8706 en_US http://dx.doi.org/10.1371/journal.pcbi.1002362 PLoS Computational Biology Creative Commons Attribution http://creativecommons.org/licenses/by/2.5/ application/pdf Public Library of Science PLoS |
| spellingShingle | Borgers, Christoph LeBeau, Fiona E. N. Boyden, Edward Stuart Kopell, Nancy J. Franzesi, Giovanni Talei Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations |
| title | Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations |
| title_full | Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations |
| title_fullStr | Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations |
| title_full_unstemmed | Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations |
| title_short | Minimal Size of Cell Assemblies Coordinated by Gamma Oscillations |
| title_sort | minimal size of cell assemblies coordinated by gamma oscillations |
| url | http://hdl.handle.net/1721.1/70468 https://orcid.org/0000-0001-7132-8706 |
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