An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity
Cholinergic modulation of cortex powerfully influences information processing and brain states, causing robust desynchronization of local field potentials and strong decorrelation of responses between neurons. In this paper, the authors reveal a somatostatin-expressing inhibitory neuron-driven corti...
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Veröffentlicht in: | Nature neuroscience 2015-06, Vol.18 (6), p.892-902 |
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description | Cholinergic modulation of cortex powerfully influences information processing and brain states, causing robust desynchronization of local field potentials and strong decorrelation of responses between neurons. In this paper, the authors reveal a somatostatin-expressing inhibitory neuron-driven cortical circuit that mediates this change in the temporal structure of cortical dynamics.
Cholinergic modulation of cortex powerfully influences information processing and brain states, causing robust desynchronization of local field potentials and strong decorrelation of responses between neurons. We found that intracortical cholinergic inputs to mouse visual cortex specifically and differentially drive a defined cortical microcircuit: they facilitate somatostatin-expressing (SOM) inhibitory neurons that in turn inhibit parvalbumin-expressing inhibitory neurons and pyramidal neurons. Selective optogenetic inhibition of SOM responses blocked desynchronization and decorrelation, demonstrating that direct cholinergic activation of SOM neurons is necessary for this phenomenon. Optogenetic inhibition of vasoactive intestinal peptide-expressing neurons did not block desynchronization, despite these neurons being activated at high levels of cholinergic drive. Direct optogenetic SOM activation, independent of cholinergic modulation, was sufficient to induce desynchronization. Together, these findings demonstrate a mechanistic basis for temporal structure in cortical populations and the crucial role of neuromodulatory drive in specific inhibitory-excitatory circuits in actively shaping the dynamics of neuronal activity. |
doi_str_mv | 10.1038/nn.4002 |
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Cholinergic modulation of cortex powerfully influences information processing and brain states, causing robust desynchronization of local field potentials and strong decorrelation of responses between neurons. We found that intracortical cholinergic inputs to mouse visual cortex specifically and differentially drive a defined cortical microcircuit: they facilitate somatostatin-expressing (SOM) inhibitory neurons that in turn inhibit parvalbumin-expressing inhibitory neurons and pyramidal neurons. Selective optogenetic inhibition of SOM responses blocked desynchronization and decorrelation, demonstrating that direct cholinergic activation of SOM neurons is necessary for this phenomenon. Optogenetic inhibition of vasoactive intestinal peptide-expressing neurons did not block desynchronization, despite these neurons being activated at high levels of cholinergic drive. Direct optogenetic SOM activation, independent of cholinergic modulation, was sufficient to induce desynchronization. Together, these findings demonstrate a mechanistic basis for temporal structure in cortical populations and the crucial role of neuromodulatory drive in specific inhibitory-excitatory circuits in actively shaping the dynamics of neuronal activity.</description><identifier>ISSN: 1097-6256</identifier><identifier>EISSN: 1546-1726</identifier><identifier>DOI: 10.1038/nn.4002</identifier><identifier>PMID: 25915477</identifier><identifier>CODEN: NANEFN</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>13/51 ; 14/19 ; 14/63 ; 14/69 ; 631/378/2613/1875 ; 631/378/3920 ; 64/110 ; 82/51 ; 9/74 ; Acetylcholine ; Acetylcholine - pharmacology ; Animal Genetics and Genomics ; Animals ; Behavioral Sciences ; Biological Techniques ; Biomedicine ; Cerebral Cortex - drug effects ; Cortical Synchronization - drug effects ; Excitatory Postsynaptic Potentials - drug effects ; Genetic aspects ; Information processing ; Interneurons - drug effects ; Mice ; Mice, Inbred C57BL ; Nerve Net - drug effects ; Neurobiology ; Neurons ; Neurons - drug effects ; Neurons - metabolism ; Neurosciences ; Optogenetics ; Parasympathetic Nervous System - drug effects ; Parvalbumins - metabolism ; Photic Stimulation ; Physiological aspects ; Pyramidal Cells - drug effects ; Somatostatin - physiology ; Vasoactive Intestinal Peptide - metabolism ; Vasoactive intestinal peptides ; Visual cortex ; Visual Pathways - drug effects</subject><ispartof>Nature neuroscience, 2015-06, Vol.18 (6), p.892-902</ispartof><rights>Springer Nature America, Inc. 2015</rights><rights>COPYRIGHT 2015 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Jun 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c630t-de62f75706e62a4f3de3d81f2b4a796027289d1edc871c0bfbbfac6218231d5e3</citedby><cites>FETCH-LOGICAL-c630t-de62f75706e62a4f3de3d81f2b4a796027289d1edc871c0bfbbfac6218231d5e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nn.4002$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nn.4002$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25915477$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Naiyan</creatorcontrib><creatorcontrib>Sugihara, Hiroki</creatorcontrib><creatorcontrib>Sur, Mriganka</creatorcontrib><title>An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity</title><title>Nature neuroscience</title><addtitle>Nat Neurosci</addtitle><addtitle>Nat Neurosci</addtitle><description>Cholinergic modulation of cortex powerfully influences information processing and brain states, causing robust desynchronization of local field potentials and strong decorrelation of responses between neurons. In this paper, the authors reveal a somatostatin-expressing inhibitory neuron-driven cortical circuit that mediates this change in the temporal structure of cortical dynamics.
Cholinergic modulation of cortex powerfully influences information processing and brain states, causing robust desynchronization of local field potentials and strong decorrelation of responses between neurons. We found that intracortical cholinergic inputs to mouse visual cortex specifically and differentially drive a defined cortical microcircuit: they facilitate somatostatin-expressing (SOM) inhibitory neurons that in turn inhibit parvalbumin-expressing inhibitory neurons and pyramidal neurons. Selective optogenetic inhibition of SOM responses blocked desynchronization and decorrelation, demonstrating that direct cholinergic activation of SOM neurons is necessary for this phenomenon. Optogenetic inhibition of vasoactive intestinal peptide-expressing neurons did not block desynchronization, despite these neurons being activated at high levels of cholinergic drive. Direct optogenetic SOM activation, independent of cholinergic modulation, was sufficient to induce desynchronization. Together, these findings demonstrate a mechanistic basis for temporal structure in cortical populations and the crucial role of neuromodulatory drive in specific inhibitory-excitatory circuits in actively shaping the dynamics of neuronal activity.</description><subject>13/51</subject><subject>14/19</subject><subject>14/63</subject><subject>14/69</subject><subject>631/378/2613/1875</subject><subject>631/378/3920</subject><subject>64/110</subject><subject>82/51</subject><subject>9/74</subject><subject>Acetylcholine</subject><subject>Acetylcholine - pharmacology</subject><subject>Animal Genetics and Genomics</subject><subject>Animals</subject><subject>Behavioral Sciences</subject><subject>Biological Techniques</subject><subject>Biomedicine</subject><subject>Cerebral Cortex - drug effects</subject><subject>Cortical Synchronization - drug effects</subject><subject>Excitatory Postsynaptic Potentials - drug effects</subject><subject>Genetic aspects</subject><subject>Information processing</subject><subject>Interneurons - 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pharmacology</topic><topic>Animal Genetics and Genomics</topic><topic>Animals</topic><topic>Behavioral Sciences</topic><topic>Biological Techniques</topic><topic>Biomedicine</topic><topic>Cerebral Cortex - drug effects</topic><topic>Cortical Synchronization - drug effects</topic><topic>Excitatory Postsynaptic Potentials - drug effects</topic><topic>Genetic aspects</topic><topic>Information processing</topic><topic>Interneurons - drug effects</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Nerve Net - drug effects</topic><topic>Neurobiology</topic><topic>Neurons</topic><topic>Neurons - drug effects</topic><topic>Neurons - metabolism</topic><topic>Neurosciences</topic><topic>Optogenetics</topic><topic>Parasympathetic Nervous System - drug effects</topic><topic>Parvalbumins - metabolism</topic><topic>Photic Stimulation</topic><topic>Physiological aspects</topic><topic>Pyramidal Cells - drug effects</topic><topic>Somatostatin - physiology</topic><topic>Vasoactive Intestinal Peptide - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Naiyan</au><au>Sugihara, Hiroki</au><au>Sur, Mriganka</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity</atitle><jtitle>Nature neuroscience</jtitle><stitle>Nat Neurosci</stitle><addtitle>Nat Neurosci</addtitle><date>2015-06-01</date><risdate>2015</risdate><volume>18</volume><issue>6</issue><spage>892</spage><epage>902</epage><pages>892-902</pages><issn>1097-6256</issn><eissn>1546-1726</eissn><coden>NANEFN</coden><abstract>Cholinergic modulation of cortex powerfully influences information processing and brain states, causing robust desynchronization of local field potentials and strong decorrelation of responses between neurons. In this paper, the authors reveal a somatostatin-expressing inhibitory neuron-driven cortical circuit that mediates this change in the temporal structure of cortical dynamics.
Cholinergic modulation of cortex powerfully influences information processing and brain states, causing robust desynchronization of local field potentials and strong decorrelation of responses between neurons. We found that intracortical cholinergic inputs to mouse visual cortex specifically and differentially drive a defined cortical microcircuit: they facilitate somatostatin-expressing (SOM) inhibitory neurons that in turn inhibit parvalbumin-expressing inhibitory neurons and pyramidal neurons. Selective optogenetic inhibition of SOM responses blocked desynchronization and decorrelation, demonstrating that direct cholinergic activation of SOM neurons is necessary for this phenomenon. Optogenetic inhibition of vasoactive intestinal peptide-expressing neurons did not block desynchronization, despite these neurons being activated at high levels of cholinergic drive. Direct optogenetic SOM activation, independent of cholinergic modulation, was sufficient to induce desynchronization. Together, these findings demonstrate a mechanistic basis for temporal structure in cortical populations and the crucial role of neuromodulatory drive in specific inhibitory-excitatory circuits in actively shaping the dynamics of neuronal activity.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>25915477</pmid><doi>10.1038/nn.4002</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 13/51 14/19 14/63 14/69 631/378/2613/1875 631/378/3920 64/110 82/51 9/74 Acetylcholine Acetylcholine - pharmacology Animal Genetics and Genomics Animals Behavioral Sciences Biological Techniques Biomedicine Cerebral Cortex - drug effects Cortical Synchronization - drug effects Excitatory Postsynaptic Potentials - drug effects Genetic aspects Information processing Interneurons - drug effects Mice Mice, Inbred C57BL Nerve Net - drug effects Neurobiology Neurons Neurons - drug effects Neurons - metabolism Neurosciences Optogenetics Parasympathetic Nervous System - drug effects Parvalbumins - metabolism Photic Stimulation Physiological aspects Pyramidal Cells - drug effects Somatostatin - physiology Vasoactive Intestinal Peptide - metabolism Vasoactive intestinal peptides Visual cortex Visual Pathways - drug effects |
title | An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity |
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