Selective Participation of Single Cortical Neurons in Neuronal Avalanches
Neuronal avalanches are scale-invariant neuronal population activity patterns in the cortex that emerge in vivo in the awake state and in vitro during balanced excitation and inhibition. Theory and experiments suggest that avalanches indicate a state of cortex that improves numerous aspects of infor...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-01-01
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| Series: | Frontiers in Neural Circuits |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncir.2020.620052/full |
| _version_ | 1818641010250481664 |
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| author | Timothy Bellay Timothy Bellay Woodrow L. Shew Shan Yu Jessica J. Falco-Walter Dietmar Plenz |
| author_facet | Timothy Bellay Timothy Bellay Woodrow L. Shew Shan Yu Jessica J. Falco-Walter Dietmar Plenz |
| author_sort | Timothy Bellay |
| collection | DOAJ |
| description | Neuronal avalanches are scale-invariant neuronal population activity patterns in the cortex that emerge in vivo in the awake state and in vitro during balanced excitation and inhibition. Theory and experiments suggest that avalanches indicate a state of cortex that improves numerous aspects of information processing by allowing for the transient and selective formation of local as well as system-wide spanning neuronal groups. If avalanches are indeed involved with information processing, one might expect that single neurons would participate in avalanche patterns selectively. Alternatively, all neurons could participate proportionally to their own activity in each avalanche as would be expected for a population rate code. Distinguishing these hypotheses, however, has been difficult as robust avalanche analysis requires technically challenging measures of their intricate organization in space and time at the population level, while also recording sub- or suprathreshold activity from individual neurons with high temporal resolution. Here, we identify repeated avalanches in the ongoing local field potential (LFP) measured with high-density microelectrode arrays in the cortex of awake nonhuman primates and in acute cortex slices from young and adult rats. We studied extracellular unit firing in vivo and intracellular responses of pyramidal neurons in vitro. We found that single neurons participate selectively in specific LFP-based avalanche patterns. Furthermore, we show in vitro that manipulating the balance of excitation and inhibition abolishes this selectivity. Our results support the view that avalanches represent the selective, scale-invariant formation of neuronal groups in line with the idea of Hebbian cell assemblies underlying cortical information processing. |
| first_indexed | 2024-12-16T23:20:22Z |
| format | Article |
| id | doaj.art-b9bf8307d02f455fbe774d7e4052d252 |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-12-16T23:20:22Z |
| publishDate | 2021-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-b9bf8307d02f455fbe774d7e4052d2522022-12-21T22:12:11ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102021-01-011410.3389/fncir.2020.620052620052Selective Participation of Single Cortical Neurons in Neuronal AvalanchesTimothy Bellay0Timothy Bellay1Woodrow L. Shew2Shan Yu3Jessica J. Falco-Walter4Dietmar Plenz5Section on Critical Brain Dynamics, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, United StatesDepartment of Neuroscience, Brown University, Providence, RI, United StatesSection on Critical Brain Dynamics, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, United StatesSection on Critical Brain Dynamics, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, United StatesSection on Critical Brain Dynamics, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, United StatesSection on Critical Brain Dynamics, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, United StatesNeuronal avalanches are scale-invariant neuronal population activity patterns in the cortex that emerge in vivo in the awake state and in vitro during balanced excitation and inhibition. Theory and experiments suggest that avalanches indicate a state of cortex that improves numerous aspects of information processing by allowing for the transient and selective formation of local as well as system-wide spanning neuronal groups. If avalanches are indeed involved with information processing, one might expect that single neurons would participate in avalanche patterns selectively. Alternatively, all neurons could participate proportionally to their own activity in each avalanche as would be expected for a population rate code. Distinguishing these hypotheses, however, has been difficult as robust avalanche analysis requires technically challenging measures of their intricate organization in space and time at the population level, while also recording sub- or suprathreshold activity from individual neurons with high temporal resolution. Here, we identify repeated avalanches in the ongoing local field potential (LFP) measured with high-density microelectrode arrays in the cortex of awake nonhuman primates and in acute cortex slices from young and adult rats. We studied extracellular unit firing in vivo and intracellular responses of pyramidal neurons in vitro. We found that single neurons participate selectively in specific LFP-based avalanche patterns. Furthermore, we show in vitro that manipulating the balance of excitation and inhibition abolishes this selectivity. Our results support the view that avalanches represent the selective, scale-invariant formation of neuronal groups in line with the idea of Hebbian cell assemblies underlying cortical information processing.https://www.frontiersin.org/articles/10.3389/fncir.2020.620052/fullnonhuman primateratprefrontal cortexprimary motor cortexhigh-density microelectrode arraylocal field potential |
| spellingShingle | Timothy Bellay Timothy Bellay Woodrow L. Shew Shan Yu Jessica J. Falco-Walter Dietmar Plenz Selective Participation of Single Cortical Neurons in Neuronal Avalanches Frontiers in Neural Circuits nonhuman primate rat prefrontal cortex primary motor cortex high-density microelectrode array local field potential |
| title | Selective Participation of Single Cortical Neurons in Neuronal Avalanches |
| title_full | Selective Participation of Single Cortical Neurons in Neuronal Avalanches |
| title_fullStr | Selective Participation of Single Cortical Neurons in Neuronal Avalanches |
| title_full_unstemmed | Selective Participation of Single Cortical Neurons in Neuronal Avalanches |
| title_short | Selective Participation of Single Cortical Neurons in Neuronal Avalanches |
| title_sort | selective participation of single cortical neurons in neuronal avalanches |
| topic | nonhuman primate rat prefrontal cortex primary motor cortex high-density microelectrode array local field potential |
| url | https://www.frontiersin.org/articles/10.3389/fncir.2020.620052/full |
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