Sleep Promotes, and Sleep Loss Inhibits, Selective Changes in Firing Rate, Response Properties and Functional Connectivity of Primary Visual Cortex Neurons
Recent studies suggest that sleep differentially alters the activity of cortical neurons based on firing rates during preceding wake—increasing the firing rates of sparsely firing neurons and decreasing those of faster firing neurons. Because sparsely firing cortical neurons may play a specialized r...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-09-01
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| Series: | Frontiers in Systems Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnsys.2018.00040/full |
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| author | Brittany C. Clawson Jaclyn Durkin Aneesha K. Suresh Emily J. Pickup Christopher G. Broussard Sara J. Aton |
| author_facet | Brittany C. Clawson Jaclyn Durkin Aneesha K. Suresh Emily J. Pickup Christopher G. Broussard Sara J. Aton |
| author_sort | Brittany C. Clawson |
| collection | DOAJ |
| description | Recent studies suggest that sleep differentially alters the activity of cortical neurons based on firing rates during preceding wake—increasing the firing rates of sparsely firing neurons and decreasing those of faster firing neurons. Because sparsely firing cortical neurons may play a specialized role in sensory processing, sleep could facilitate sensory function via selective actions on sparsely firing neurons. To test this hypothesis, we analyzed longitudinal electrophysiological recordings of primary visual cortex (V1) neurons across a novel visual experience which induces V1 plasticity (or a control experience which does not), and a period of subsequent ad lib sleep or partial sleep deprivation. We find that across a day of ad lib sleep, spontaneous and visually-evoked firing rates are selectively augmented in sparsely firing V1 neurons. These sparsely firing neurons are more highly visually responsive, and show greater orientation selectivity than their high firing rate neighbors. They also tend to be “soloists” instead of “choristers”—showing relatively weak coupling of firing to V1 population activity. These population-specific changes in firing rate are blocked by sleep disruption either early or late in the day, and appear to be brought about by increases in neuronal firing rates across bouts of rapid eye movement (REM) sleep. Following a patterned visual experience that induces orientation-selective response potentiation (OSRP) in V1, sparsely firing and weakly population-coupled neurons show the highest level of sleep-dependent response plasticity. Across a day of ad lib sleep, population coupling strength increases selectively for sparsely firing neurons—this effect is also disrupted by sleep deprivation. Together, these data suggest that sleep may optimize sensory function by augmenting the functional connectivity and firing rate of highly responsive and stimulus-selective cortical neurons, while simultaneously reducing noise in the network by decreasing the activity of less selective, faster-firing neurons. |
| first_indexed | 2024-12-11T17:46:14Z |
| format | Article |
| id | doaj.art-225e51aad5134a6583de5eed5cc58837 |
| institution | Directory Open Access Journal |
| issn | 1662-5137 |
| language | English |
| last_indexed | 2024-12-11T17:46:14Z |
| publishDate | 2018-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Systems Neuroscience |
| spelling | doaj.art-225e51aad5134a6583de5eed5cc588372022-12-22T00:56:22ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372018-09-011210.3389/fnsys.2018.00040403499Sleep Promotes, and Sleep Loss Inhibits, Selective Changes in Firing Rate, Response Properties and Functional Connectivity of Primary Visual Cortex NeuronsBrittany C. Clawson0Jaclyn Durkin1Aneesha K. Suresh2Emily J. Pickup3Christopher G. Broussard4Sara J. Aton5Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, United StatesNeuroscience Graduate Program, University of Michigan, Ann Arbor, MI, United StatesCommittee on Computational Neuroscience, University of Chicago, Chicago, IL, United StatesDepartment of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, United StatesInformation Technology Advocacy and Research Support, College of Literature, Science and the Arts, University of Michigan, Ann Arbor, MI, United StatesDepartment of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, United StatesRecent studies suggest that sleep differentially alters the activity of cortical neurons based on firing rates during preceding wake—increasing the firing rates of sparsely firing neurons and decreasing those of faster firing neurons. Because sparsely firing cortical neurons may play a specialized role in sensory processing, sleep could facilitate sensory function via selective actions on sparsely firing neurons. To test this hypothesis, we analyzed longitudinal electrophysiological recordings of primary visual cortex (V1) neurons across a novel visual experience which induces V1 plasticity (or a control experience which does not), and a period of subsequent ad lib sleep or partial sleep deprivation. We find that across a day of ad lib sleep, spontaneous and visually-evoked firing rates are selectively augmented in sparsely firing V1 neurons. These sparsely firing neurons are more highly visually responsive, and show greater orientation selectivity than their high firing rate neighbors. They also tend to be “soloists” instead of “choristers”—showing relatively weak coupling of firing to V1 population activity. These population-specific changes in firing rate are blocked by sleep disruption either early or late in the day, and appear to be brought about by increases in neuronal firing rates across bouts of rapid eye movement (REM) sleep. Following a patterned visual experience that induces orientation-selective response potentiation (OSRP) in V1, sparsely firing and weakly population-coupled neurons show the highest level of sleep-dependent response plasticity. Across a day of ad lib sleep, population coupling strength increases selectively for sparsely firing neurons—this effect is also disrupted by sleep deprivation. Together, these data suggest that sleep may optimize sensory function by augmenting the functional connectivity and firing rate of highly responsive and stimulus-selective cortical neurons, while simultaneously reducing noise in the network by decreasing the activity of less selective, faster-firing neurons.https://www.frontiersin.org/article/10.3389/fnsys.2018.00040/fullin vivo recordingsensory cortexexcitabilityinformation processingsignal-to-noise |
| spellingShingle | Brittany C. Clawson Jaclyn Durkin Aneesha K. Suresh Emily J. Pickup Christopher G. Broussard Sara J. Aton Sleep Promotes, and Sleep Loss Inhibits, Selective Changes in Firing Rate, Response Properties and Functional Connectivity of Primary Visual Cortex Neurons Frontiers in Systems Neuroscience in vivo recording sensory cortex excitability information processing signal-to-noise |
| title | Sleep Promotes, and Sleep Loss Inhibits, Selective Changes in Firing Rate, Response Properties and Functional Connectivity of Primary Visual Cortex Neurons |
| title_full | Sleep Promotes, and Sleep Loss Inhibits, Selective Changes in Firing Rate, Response Properties and Functional Connectivity of Primary Visual Cortex Neurons |
| title_fullStr | Sleep Promotes, and Sleep Loss Inhibits, Selective Changes in Firing Rate, Response Properties and Functional Connectivity of Primary Visual Cortex Neurons |
| title_full_unstemmed | Sleep Promotes, and Sleep Loss Inhibits, Selective Changes in Firing Rate, Response Properties and Functional Connectivity of Primary Visual Cortex Neurons |
| title_short | Sleep Promotes, and Sleep Loss Inhibits, Selective Changes in Firing Rate, Response Properties and Functional Connectivity of Primary Visual Cortex Neurons |
| title_sort | sleep promotes and sleep loss inhibits selective changes in firing rate response properties and functional connectivity of primary visual cortex neurons |
| topic | in vivo recording sensory cortex excitability information processing signal-to-noise |
| url | https://www.frontiersin.org/article/10.3389/fnsys.2018.00040/full |
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