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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Bibliographic Details
Published in:Nature neuroscience Vol. 23; no. 7; pp. 892 - 902
Main Authors: Cho, Kathleen K A, Davidson, Thomas J, Bouvier, Guy, Marshall, Jesse D, Schnitzer, Mark J, Sohal, Vikaas S
Format: Journal Article
Language:English
Published: United States Nature Publishing Group 01.07.2020
Subjects:
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
Online Access:Get full text
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Summary: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gamma synchrony between PV interneurons when mice received feedback that previously learned associations were no longer valid. Disrupting this synchronization by delivering out-of-phase optogenetic stimulation caused mice to perseverate on outdated associations, an effect not reproduced by in-phase stimulation or out-of-phase stimulation at other frequencies.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.
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ISSN:1097-6256
1546-1726
1546-1726
DOI:10.1038/s41593-020-0647-1