Cross-hemispheric gamma synchrony between prefrontal parvalbumin interneurons supports behavioral adaptation during rule shift learning

Organisms must learn new strategies to adapt to changing environments. Activity in different neurons often exhibits synchronization that can dynamically enhance their communication and might create flexible brain states that facilitate changes in behavior. We studied the role of gamma-frequency (~40...

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Vydané v:Nature neuroscience Ročník 23; číslo 7; s. 892 - 902
Hlavní autori: Cho, Kathleen K A, Davidson, Thomas J, Bouvier, Guy, Marshall, Jesse D, Schnitzer, Mark J, Sohal, Vikaas S
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Nature Publishing Group 01.07.2020
Predmet:
Adaptation
Adaptation, Physiological - physiology
Animals
Association Learning - physiology
Behavior
Changing environments
Cues
Female
Frequency synchronization
Functional Laterality
Gamma Rhythm - physiology
Interneurons
Interneurons - physiology
Learning
Male
Mice
Neurosciences
Parvalbumin
Parvalbumins - metabolism
Prefrontal cortex
Prefrontal Cortex - physiology
Reinforcement
Reward
Stimulation
Synchronization
Voltage indicators
ISSN:1097-6256, 1546-1726, 1546-1726
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Abstract Organisms must learn new strategies to adapt to changing environments. Activity in different neurons often exhibits synchronization that can dynamically enhance their communication and might create flexible brain states that facilitate changes in behavior. We studied the role of gamma-frequency (~40 Hz) synchrony between prefrontal parvalbumin (PV) interneurons in mice learning multiple new cue-reward associations. Voltage indicators revealed cell-type-specific increases of cross-hemispheric gamma synchrony between PV interneurons when mice received feedback that previously learned associations were no longer valid. Disrupting this synchronization by delivering out-of-phase optogenetic stimulation caused mice to perseverate on outdated associations, an effect not reproduced by in-phase stimulation or out-of-phase stimulation at other frequencies. Gamma synchrony was specifically required when new associations used familiar cues that were previously irrelevant to behavioral outcomes, not when associations involved new cues or for reversing previously learned associations. Thus, gamma synchrony is indispensable for reappraising the behavioral salience of external cues.
AbstractList Organisms must learn new strategies to adapt to changing environments. Activity in different neurons often exhibits synchronization that can dynamically enhance their communication and might create flexible brain states that facilitate changes in behavior. We studied the role of gamma-frequency (~40 Hz) synchrony between prefrontal parvalbumin (PV) interneurons in mice learning multiple new cue–reward associations. Voltage indicators revealed cell-type-specific increases of cross-hemispheric gamma synchrony between PV interneurons when mice received feedback that previously learned associations were no longer valid. Disrupting this synchronization by delivering out-of-phase optogenetic stimulation caused mice to perseverate on outdated associations, an effect not reproduced by in-phase stimulation or out-of-phase stimulation at other frequencies. Gamma synchrony was specifically required when new associations used familiar cues that were previously irrelevant to behavioral outcomes, not when associations involved new cues or for reversing previously learned associations. Thus, gamma synchrony is indispensable for reappraising the behavioral salience of external cues.Learning new associations that reappraise the behavioral significance of previously irrelevant cues requires gamma-frequency synchronization between parvalbumin interneurons in the left and right prefrontal cortex.
Organisms must learn new strategies to adapt to changing environments. Activity in different neurons often exhibits synchronization that can dynamically enhance their communication and might create flexible brain states that facilitate changes in behavior. We studied the role of gamma-frequency (~40 Hz) synchrony between prefrontal parvalbumin (PV) interneurons in mice learning multiple new cue-reward associations. Voltage indicators revealed cell-type-specific increases of cross-hemispheric gamma synchrony between PV interneurons when mice received feedback that previously learned associations were no longer valid. Disrupting this synchronization by delivering out-of-phase optogenetic stimulation caused mice to perseverate on outdated associations, an effect not reproduced by in-phase stimulation or out-of-phase stimulation at other frequencies. Gamma synchrony was specifically required when new associations used familiar cues that were previously irrelevant to behavioral outcomes, not when associations involved new cues or for reversing previously learned associations. Thus, gamma synchrony is indispensable for reappraising the behavioral salience of external cues.
Organisms must learn new strategies to adapt to changing environments. Activity in different neurons often exhibits synchronization that can dynamically enhance their communication and might create flexible brain states that facilitate changes in behavior. We studied the role of gamma-frequency (~40 Hz) synchrony between prefrontal parvalbumin (PV) interneurons in mice learning multiple new cue-reward associations. Voltage indicators revealed cell-type-specific increases of cross-hemispheric gamma synchrony between PV interneurons when mice received feedback that previously learned associations were no longer valid. Disrupting this synchronization by delivering out-of-phase optogenetic stimulation caused mice to perseverate on outdated associations, an effect not reproduced by in-phase stimulation or out-of-phase stimulation at other frequencies. Gamma synchrony was specifically required when new associations used familiar cues that were previously irrelevant to behavioral outcomes, not when associations involved new cues or for reversing previously learned associations. Thus, gamma synchrony is indispensable for reappraising the behavioral salience of external cues.Organisms must learn new strategies to adapt to changing environments. Activity in different neurons often exhibits synchronization that can dynamically enhance their communication and might create flexible brain states that facilitate changes in behavior. We studied the role of gamma-frequency (~40 Hz) synchrony between prefrontal parvalbumin (PV) interneurons in mice learning multiple new cue-reward associations. Voltage indicators revealed cell-type-specific increases of cross-hemispheric gamma synchrony between PV interneurons when mice received feedback that previously learned associations were no longer valid. Disrupting this synchronization by delivering out-of-phase optogenetic stimulation caused mice to perseverate on outdated associations, an effect not reproduced by in-phase stimulation or out-of-phase stimulation at other frequencies. Gamma synchrony was specifically required when new associations used familiar cues that were previously irrelevant to behavioral outcomes, not when associations involved new cues or for reversing previously learned associations. Thus, gamma synchrony is indispensable for reappraising the behavioral salience of external cues.
Author Bouvier, Guy
Davidson, Thomas J
Marshall, Jesse D
Cho, Kathleen K A
Schnitzer, Mark J
Sohal, Vikaas S
Author_xml – sequence: 1
  givenname: Kathleen K A
  orcidid: 0000-0003-0215-8779
  surname: Cho
  fullname: Cho, Kathleen K A
  organization: Weill Institute for Neuroscience, University of California, San Francisco, San Francisco, CA, USA
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  givenname: Thomas J
  orcidid: 0000-0003-0836-6333
  surname: Davidson
  fullname: Davidson, Thomas J
  organization: Howard Hughes Medical Institute, San Francisco, CA, USA
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  givenname: Guy
  orcidid: 0000-0002-6160-7186
  surname: Bouvier
  fullname: Bouvier, Guy
  organization: Howard Hughes Medical Institute, San Francisco, CA, USA
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  givenname: Jesse D
  orcidid: 0000-0003-4810-6712
  surname: Marshall
  fullname: Marshall, Jesse D
  organization: Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, MA, USA
– sequence: 5
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  orcidid: 0000-0002-2238-4186
  surname: Sohal
  fullname: Sohal, Vikaas S
  email: vikaas.sohal@ucsf.edu, vikaas.sohal@ucsf.edu, vikaas.sohal@ucsf.edu
  organization: Weill Institute for Neuroscience, University of California, San Francisco, San Francisco, CA, USA. vikaas.sohal@ucsf.edu
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Snippet Organisms must learn new strategies to adapt to changing environments. Activity in different neurons often exhibits synchronization that can dynamically...
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SubjectTerms Adaptation
Adaptation, Physiological - physiology
Animals
Association Learning - physiology
Behavior
Changing environments
Cues
Female
Frequency synchronization
Functional Laterality
Gamma Rhythm - physiology
Interneurons
Interneurons - physiology
Learning
Male
Mice
Neurosciences
Parvalbumin
Parvalbumins - metabolism
Prefrontal cortex
Prefrontal Cortex - physiology
Reinforcement
Reward
Stimulation
Synchronization
Voltage indicators
Title Cross-hemispheric gamma synchrony between prefrontal parvalbumin interneurons supports behavioral adaptation during rule shift learning
URI https://www.ncbi.nlm.nih.gov/pubmed/32451483
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