Origin of Active States in Local Neocortical Networks during Slow Sleep Oscillation
Slow-wave sleep is characterized by spontaneous alternations of activity and silence in corticothalamic networks, but the causes of transition from silence to activity remain unknown. We investigated local mechanisms underlying initiation of activity, using simultaneous multisite field potential, mu...
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| Published in | Cerebral cortex (New York, N.Y. 1991) Vol. 20; no. 11; pp. 2660 - 2674 |
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| Main Authors | , , |
| Format | Journal Article |
| Language | English |
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United States
Oxford University Press
01.11.2010
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| Abstract | Slow-wave sleep is characterized by spontaneous alternations of activity and silence in corticothalamic networks, but the causes of transition from silence to activity remain unknown. We investigated local mechanisms underlying initiation of activity, using simultaneous multisite field potential, multiunit recordings, and intracellular recordings from 2 to 4 nearby neurons in naturally sleeping or anesthetized cats. We demonstrate that activity may start in any neuron or recording location, with tens of milliseconds delay in other cells and sites. Typically, however, activity originated at deep locations, then involved some superficial cells, but appeared later in the middle of the cortex. Neuronal firing was also found to begin, after the onset of active states, at depths that correspond to cortical layer V. These results support the hypothesis that switch from silence to activity is mediated by spontaneous synaptic events, whereby any neuron may become active first. Due to probabilistic nature of activity onset, the large pyramidal cells from deep cortical layers, which are equipped with the most numerous synaptic inputs and large projection fields, are best suited for switching the whole network into active state. |
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| AbstractList | Slow-wave sleep is characterized by spontaneous alternations of activity and silence in corticothalamic networks, but the causes of transition from silence to activity remain unknown. We investigated local mechanisms underlying initiation of activity, using simultaneous multisite field potential, multiunit recordings, and intracellular recordings from 2 to 4 nearby neurons in naturally sleeping or anesthetized cats. We demonstrate that activity may start in any neuron or recording location, with tens of milliseconds delay in other cells and sites. Typically, however, activity originated at deep locations, then involved some superficial cells, but appeared later in the middle of the cortex. Neuronal firing was also found to begin, after the onset of active states, at depths that correspond to cortical layer V. These results support the hypothesis that switch from silence to activity is mediated by spontaneous synaptic events, whereby any neuron may become active first. Due to probabilistic nature of activity onset, the large pyramidal cells from deep cortical layers, which are equipped with the most numerous synaptic inputs and large projection fields, are best suited for switching the whole network into active state. Slow-wave sleep is characterized by spontaneous alternations of activity and silence in corticothalamic networks, but the causes of transition from silence to activity remain unknown. We investigated local mechanisms underlying initiation of activity, using simultaneous multisite field potential, multiunit recordings, and intracellular recordings from 2 to 4 nearby neurons in naturally sleeping or anesthetized cats. We demonstrate that activity may start in any neuron or recording location, with tens of milliseconds delay in other cells and sites. Typically, however, activity originated at deep locations, then involved some superficial cells, but appeared later in the middle of the cortex. Neuronal firing was also found to begin, after the onset of active states, at depths that correspond to cortical layer V. These results support the hypothesis that switch from silence to activity is mediated by spontaneous synaptic events, whereby any neuron may become active first. Due to probabilistic nature of activity onset, the large pyramidal cells from deep cortical layers, which are equipped with the most numerous synaptic inputs and large projection fields, are best suited for switching the whole network into active state.Slow-wave sleep is characterized by spontaneous alternations of activity and silence in corticothalamic networks, but the causes of transition from silence to activity remain unknown. We investigated local mechanisms underlying initiation of activity, using simultaneous multisite field potential, multiunit recordings, and intracellular recordings from 2 to 4 nearby neurons in naturally sleeping or anesthetized cats. We demonstrate that activity may start in any neuron or recording location, with tens of milliseconds delay in other cells and sites. Typically, however, activity originated at deep locations, then involved some superficial cells, but appeared later in the middle of the cortex. Neuronal firing was also found to begin, after the onset of active states, at depths that correspond to cortical layer V. These results support the hypothesis that switch from silence to activity is mediated by spontaneous synaptic events, whereby any neuron may become active first. Due to probabilistic nature of activity onset, the large pyramidal cells from deep cortical layers, which are equipped with the most numerous synaptic inputs and large projection fields, are best suited for switching the whole network into active state. |
| Author | Timofeev, Igor Volgushev, Maxim Chauvette, Sylvain |
| AuthorAffiliation | 3 Department Cellular Biology of Learning, Institute of Higher Nervous Activity and Neurophysiology, Moscow 117485, Russia 1 Department of Psychiatry and Neuroscience, The Centre de Recherche Université Laval Robert-Giffard (CRULRG), Laval University, Québec, PQ, Canada G1J 2G3 4 Department of Psychology, University of Connecticut, Storrs, CT 06269-1020, USA 2 Department of Neurophysiology, Ruhr-University Bochum, Bochum, D-44780, Germany |
| AuthorAffiliation_xml | – name: 1 Department of Psychiatry and Neuroscience, The Centre de Recherche Université Laval Robert-Giffard (CRULRG), Laval University, Québec, PQ, Canada G1J 2G3 – name: 2 Department of Neurophysiology, Ruhr-University Bochum, Bochum, D-44780, Germany – name: 4 Department of Psychology, University of Connecticut, Storrs, CT 06269-1020, USA – name: 3 Department Cellular Biology of Learning, Institute of Higher Nervous Activity and Neurophysiology, Moscow 117485, Russia |
| Author_xml | – sequence: 1 givenname: Sylvain surname: Chauvette fullname: Chauvette, Sylvain organization: Department of Psychiatry and Neuroscience, The Centre de Recherche Université Laval Robert-Giffard (CRULRG), Laval University, Québec, PQ, Canada G1J 2G3 – sequence: 2 givenname: Maxim surname: Volgushev fullname: Volgushev, Maxim organization: Department of Neurophysiology, Ruhr-University Bochum, Bochum, D-44780, Germany – sequence: 3 givenname: Igor surname: Timofeev fullname: Timofeev, Igor email: igor.timofeev@phs.ulaval.ca organization: Department of Psychiatry and Neuroscience, The Centre de Recherche Université Laval Robert-Giffard (CRULRG), Laval University, Québec, PQ, Canada G1J 2G3 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20200108$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Action Potentials - physiology Animals Biological Clocks - physiology Cats Female intracellular intrinsic Male Neocortex - anatomy & histology Neocortex - cytology Neocortex - physiology Nerve Net - anatomy & histology Nerve Net - cytology Nerve Net - physiology Neurons - cytology Neurons - physiology oscillations sleep Sleep - physiology synaptic synchronization |
| Title | Origin of Active States in Local Neocortical Networks during Slow Sleep Oscillation |
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