Thirst regulates motivated behavior through modulation of brainwide neural population dynamics
Physiological needs produce motivational drives, such as thirst and hunger, that regulate behaviors essential to survival. Hypothalamic neurons sense these needs and must coordinate relevant brainwide neuronal activity to produce the appropriate behavior. We studied dynamics from ~24,000 neurons in...
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Veröffentlicht in: | Science (American Association for the Advancement of Science) 2019-04, Vol.364 (6437), p.253-253 |
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creator | Allen, William E. Chen, Michael Z. Pichamoorthy, Nandini Tien, Rebecca H. Pachitariu, Marius Luo, Liqun Deisseroth, Karl |
description | Physiological needs produce motivational drives, such as thirst and hunger, that regulate behaviors essential to survival. Hypothalamic neurons sense these needs and must coordinate relevant brainwide neuronal activity to produce the appropriate behavior. We studied dynamics from ~24,000 neurons in 34 brain regions during thirst-motivated choice behavior in 21 mice as they consumed water and became sated. Water-predicting sensory cues elicited activity that rapidly spread throughout the brain of thirsty animals. These dynamics were gated by a brainwide mode of population activity that encoded motivational state. After satiation, focal optogenetic activation of hypothalamic thirst-sensing neurons returned global activity to the pre-satiation state. Thus, motivational states specify initial conditions that determine how a brainwide dynamical system transforms sensory input into behavioral output. |
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Hypothalamic neurons sense these needs and must coordinate relevant brainwide neuronal activity to produce the appropriate behavior. We studied dynamics from ~24,000 neurons in 34 brain regions during thirst-motivated choice behavior in 21 mice as they consumed water and became sated. Water-predicting sensory cues elicited activity that rapidly spread throughout the brain of thirsty animals. These dynamics were gated by a brainwide mode of population activity that encoded motivational state. After satiation, focal optogenetic activation of hypothalamic thirst-sensing neurons returned global activity to the pre-satiation state. Thus, motivational states specify initial conditions that determine how a brainwide dynamical system transforms sensory input into behavioral output.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.aav3932</identifier><identifier>PMID: 30948440</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Amygdala ; Animal behavior ; Animals ; Anxiety ; Arousal ; Behavior ; Brain ; Choice Behavior - physiology ; Coding ; Correlation ; Decision making ; Drinking water ; Dynamics ; Electrophysiological recording ; Exploratory behavior ; Feedback (Response) ; Female ; Flow mapping ; Hunger ; Hypothalamus ; Hypothalamus - cytology ; Hypothalamus - physiology ; Initial conditions ; Mice ; Mice, Inbred C57BL ; Motivation ; Motor activity ; Motor task performance ; Neural networks ; Neural Pathways - physiology ; Neurons ; Neurons - physiology ; Odor ; Odors ; Olfactory pathways ; Optogenetics ; Physiology ; Recording ; Representations ; RESEARCH ARTICLE SUMMARY ; Satiety ; Sensorimotor integration ; Sensory evaluation ; Sensory Receptor Cells - physiology ; Sensory stimulation ; Single-Cell Analysis ; Somatosensory cortex ; Stimuli ; Survival ; Technology ; Thirst ; Thirst - physiology ; Visual cortex ; Visual stimuli ; Water</subject><ispartof>Science (American Association for the Advancement of Science), 2019-04, Vol.364 (6437), p.253-253</ispartof><rights>Copyright © 2019, American Association for the Advancement of Science.</rights><rights>Copyright © 2019, American Association for the Advancement of Science</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-c603e565c2e7e5ab9c4ab3b94f650c7f95ed5b77eb41f6557acb3b0b771685d63</citedby><cites>FETCH-LOGICAL-c509t-c603e565c2e7e5ab9c4ab3b94f650c7f95ed5b77eb41f6557acb3b0b771685d63</cites><orcidid>0000-0002-3674-666X ; 0000-0002-2998-9014 ; 0000-0001-9590-953X ; 0000-0001-9440-3967 ; 0000-0001-7106-814X ; 0000-0001-5467-9264 ; 0000-0001-6969-9911</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,2870,2871,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30948440$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Allen, William E.</creatorcontrib><creatorcontrib>Chen, Michael Z.</creatorcontrib><creatorcontrib>Pichamoorthy, Nandini</creatorcontrib><creatorcontrib>Tien, Rebecca H.</creatorcontrib><creatorcontrib>Pachitariu, Marius</creatorcontrib><creatorcontrib>Luo, Liqun</creatorcontrib><creatorcontrib>Deisseroth, Karl</creatorcontrib><title>Thirst regulates motivated behavior through modulation of brainwide neural population dynamics</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Physiological needs produce motivational drives, such as thirst and hunger, that regulate behaviors essential to survival. Hypothalamic neurons sense these needs and must coordinate relevant brainwide neuronal activity to produce the appropriate behavior. We studied dynamics from ~24,000 neurons in 34 brain regions during thirst-motivated choice behavior in 21 mice as they consumed water and became sated. Water-predicting sensory cues elicited activity that rapidly spread throughout the brain of thirsty animals. These dynamics were gated by a brainwide mode of population activity that encoded motivational state. After satiation, focal optogenetic activation of hypothalamic thirst-sensing neurons returned global activity to the pre-satiation state. Thus, motivational states specify initial conditions that determine how a brainwide dynamical system transforms sensory input into behavioral output.</description><subject>Amygdala</subject><subject>Animal behavior</subject><subject>Animals</subject><subject>Anxiety</subject><subject>Arousal</subject><subject>Behavior</subject><subject>Brain</subject><subject>Choice Behavior - physiology</subject><subject>Coding</subject><subject>Correlation</subject><subject>Decision making</subject><subject>Drinking water</subject><subject>Dynamics</subject><subject>Electrophysiological recording</subject><subject>Exploratory behavior</subject><subject>Feedback (Response)</subject><subject>Female</subject><subject>Flow mapping</subject><subject>Hunger</subject><subject>Hypothalamus</subject><subject>Hypothalamus - cytology</subject><subject>Hypothalamus - physiology</subject><subject>Initial conditions</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Motivation</subject><subject>Motor activity</subject><subject>Motor task performance</subject><subject>Neural networks</subject><subject>Neural Pathways - physiology</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Odor</subject><subject>Odors</subject><subject>Olfactory pathways</subject><subject>Optogenetics</subject><subject>Physiology</subject><subject>Recording</subject><subject>Representations</subject><subject>RESEARCH ARTICLE SUMMARY</subject><subject>Satiety</subject><subject>Sensorimotor integration</subject><subject>Sensory evaluation</subject><subject>Sensory Receptor Cells - physiology</subject><subject>Sensory stimulation</subject><subject>Single-Cell Analysis</subject><subject>Somatosensory cortex</subject><subject>Stimuli</subject><subject>Survival</subject><subject>Technology</subject><subject>Thirst</subject><subject>Thirst - physiology</subject><subject>Visual cortex</subject><subject>Visual stimuli</subject><subject>Water</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU1r3DAQhkVpaLZpzz21GHrpxcnI-lpdCiX0IxDIJb1WyPJ4rcWWtpK9Jf--CrtZ2pw0zPNomOEl5B2FS0obeZWdx-Dw0to906x5QVYUtKh1A-wlWQEwWa9BiXPyOuctQGGavSLnDDRfcw4r8ut-8CnPVcLNMtoZczXF2e9L1VUtDnbvY6rmIcVlMxTUPUo-hir2VZusD398h1XAJdmx2sXdE-4egp28y2_IWW_HjG-P7wX5-e3r_fWP-vbu-831l9vaCdBz7SQwFFK4BhUK22rHbctazXspwKleC-xEqxS2nJaWUNYVDKVD5Vp0kl2Qz4e5u6WdsHMY5rKR2SU_2fRgovXmfxL8YDZxb6SilKumDPh0HJDi7wXzbCafHY6jDRiXbJoGuNSMKyjqx2fqNi4plPOKRSmT0AhVrKuD5VLMOWF_WoaCeczOHLMzx-zKjw__3nDyn8IqwvuDsM1zTCfeSMk1Y5L9BbICpFY</recordid><startdate>20190419</startdate><enddate>20190419</enddate><creator>Allen, William E.</creator><creator>Chen, Michael Z.</creator><creator>Pichamoorthy, Nandini</creator><creator>Tien, Rebecca H.</creator><creator>Pachitariu, Marius</creator><creator>Luo, Liqun</creator><creator>Deisseroth, Karl</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3674-666X</orcidid><orcidid>https://orcid.org/0000-0002-2998-9014</orcidid><orcidid>https://orcid.org/0000-0001-9590-953X</orcidid><orcidid>https://orcid.org/0000-0001-9440-3967</orcidid><orcidid>https://orcid.org/0000-0001-7106-814X</orcidid><orcidid>https://orcid.org/0000-0001-5467-9264</orcidid><orcidid>https://orcid.org/0000-0001-6969-9911</orcidid></search><sort><creationdate>20190419</creationdate><title>Thirst regulates motivated behavior through modulation of brainwide neural population dynamics</title><author>Allen, William E. ; Chen, Michael Z. ; Pichamoorthy, Nandini ; Tien, Rebecca H. ; Pachitariu, Marius ; Luo, Liqun ; Deisseroth, Karl</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c509t-c603e565c2e7e5ab9c4ab3b94f650c7f95ed5b77eb41f6557acb3b0b771685d63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Amygdala</topic><topic>Animal behavior</topic><topic>Animals</topic><topic>Anxiety</topic><topic>Arousal</topic><topic>Behavior</topic><topic>Brain</topic><topic>Choice Behavior - physiology</topic><topic>Coding</topic><topic>Correlation</topic><topic>Decision making</topic><topic>Drinking water</topic><topic>Dynamics</topic><topic>Electrophysiological recording</topic><topic>Exploratory behavior</topic><topic>Feedback (Response)</topic><topic>Female</topic><topic>Flow mapping</topic><topic>Hunger</topic><topic>Hypothalamus</topic><topic>Hypothalamus - cytology</topic><topic>Hypothalamus - physiology</topic><topic>Initial conditions</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Motivation</topic><topic>Motor activity</topic><topic>Motor task performance</topic><topic>Neural networks</topic><topic>Neural Pathways - physiology</topic><topic>Neurons</topic><topic>Neurons - physiology</topic><topic>Odor</topic><topic>Odors</topic><topic>Olfactory pathways</topic><topic>Optogenetics</topic><topic>Physiology</topic><topic>Recording</topic><topic>Representations</topic><topic>RESEARCH ARTICLE SUMMARY</topic><topic>Satiety</topic><topic>Sensorimotor integration</topic><topic>Sensory evaluation</topic><topic>Sensory Receptor Cells - physiology</topic><topic>Sensory stimulation</topic><topic>Single-Cell Analysis</topic><topic>Somatosensory cortex</topic><topic>Stimuli</topic><topic>Survival</topic><topic>Technology</topic><topic>Thirst</topic><topic>Thirst - physiology</topic><topic>Visual cortex</topic><topic>Visual stimuli</topic><topic>Water</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Allen, William E.</creatorcontrib><creatorcontrib>Chen, Michael Z.</creatorcontrib><creatorcontrib>Pichamoorthy, Nandini</creatorcontrib><creatorcontrib>Tien, Rebecca H.</creatorcontrib><creatorcontrib>Pachitariu, Marius</creatorcontrib><creatorcontrib>Luo, Liqun</creatorcontrib><creatorcontrib>Deisseroth, Karl</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Allen, William E.</au><au>Chen, Michael Z.</au><au>Pichamoorthy, Nandini</au><au>Tien, Rebecca H.</au><au>Pachitariu, Marius</au><au>Luo, Liqun</au><au>Deisseroth, Karl</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Thirst regulates motivated behavior through modulation of brainwide neural population dynamics</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2019-04-19</date><risdate>2019</risdate><volume>364</volume><issue>6437</issue><spage>253</spage><epage>253</epage><pages>253-253</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><abstract>Physiological needs produce motivational drives, such as thirst and hunger, that regulate behaviors essential to survival. Hypothalamic neurons sense these needs and must coordinate relevant brainwide neuronal activity to produce the appropriate behavior. We studied dynamics from ~24,000 neurons in 34 brain regions during thirst-motivated choice behavior in 21 mice as they consumed water and became sated. Water-predicting sensory cues elicited activity that rapidly spread throughout the brain of thirsty animals. These dynamics were gated by a brainwide mode of population activity that encoded motivational state. After satiation, focal optogenetic activation of hypothalamic thirst-sensing neurons returned global activity to the pre-satiation state. Thus, motivational states specify initial conditions that determine how a brainwide dynamical system transforms sensory input into behavioral output.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>30948440</pmid><doi>10.1126/science.aav3932</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-3674-666X</orcidid><orcidid>https://orcid.org/0000-0002-2998-9014</orcidid><orcidid>https://orcid.org/0000-0001-9590-953X</orcidid><orcidid>https://orcid.org/0000-0001-9440-3967</orcidid><orcidid>https://orcid.org/0000-0001-7106-814X</orcidid><orcidid>https://orcid.org/0000-0001-5467-9264</orcidid><orcidid>https://orcid.org/0000-0001-6969-9911</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amygdala Animal behavior Animals Anxiety Arousal Behavior Brain Choice Behavior - physiology Coding Correlation Decision making Drinking water Dynamics Electrophysiological recording Exploratory behavior Feedback (Response) Female Flow mapping Hunger Hypothalamus Hypothalamus - cytology Hypothalamus - physiology Initial conditions Mice Mice, Inbred C57BL Motivation Motor activity Motor task performance Neural networks Neural Pathways - physiology Neurons Neurons - physiology Odor Odors Olfactory pathways Optogenetics Physiology Recording Representations RESEARCH ARTICLE SUMMARY Satiety Sensorimotor integration Sensory evaluation Sensory Receptor Cells - physiology Sensory stimulation Single-Cell Analysis Somatosensory cortex Stimuli Survival Technology Thirst Thirst - physiology Visual cortex Visual stimuli Water |
title | Thirst regulates motivated behavior through modulation of brainwide neural population dynamics |
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