Laboratory of 3D functional network and dendritic imaging, Institute of Experimental Medicine, Budapest, Hungary; MTA-PPKE ITK-NAP B – 2p Measurement Technology Group, The Faculty of Information Technology, Pázmány Péter Catholic University, Budapest, Hungary; János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, Hungary; BrainVisionCenter, Budapest, Hungary
Hyun-Jae Pi
Cold Spring Harbor Laboratory, Cold Spring Harbor, United States; Volen Center for Complex Systems, Biology Department, Brandeis University, Waltham, United States
Quentin Chevy
Cold Spring Harbor Laboratory, Cold Spring Harbor, United States; Departments of Neuroscience and Psychiatry, Washington University School of Medicine, St. Louis, United States
Katalin Ócsai
MTA-PPKE ITK-NAP B – 2p Measurement Technology Group, The Faculty of Information Technology, Pázmány Péter Catholic University, Budapest, Hungary; BrainVisionCenter, Budapest, Hungary; Computational Systems Neuroscience Lab, Wigner Research Centre for Physics, Budapest, Hungary; Department of Mathematical Geometry, Institute of Mathematics, Budapest University of Technology and Economics, Budapest, Hungary
Dinu F Albeanu
Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
Balázs Chiovini
Laboratory of 3D functional network and dendritic imaging, Institute of Experimental Medicine, Budapest, Hungary
Gergely Szalay
Laboratory of 3D functional network and dendritic imaging, Institute of Experimental Medicine, Budapest, Hungary
Gergely Katona
MTA-PPKE ITK-NAP B – 2p Measurement Technology Group, The Faculty of Information Technology, Pázmány Péter Catholic University, Budapest, Hungary
Adam Kepecs
Cold Spring Harbor Laboratory, Cold Spring Harbor, United States; Departments of Neuroscience and Psychiatry, Washington University School of Medicine, St. Louis, United States
Neocortex is classically divided into distinct areas, each specializing in different function, but all could benefit from reinforcement feedback to inform and update local processing. Yet it remains elusive how global signals like reward and punishment are represented in local cortical computations. Previously, we identified a cortical neuron type, vasoactive intestinal polypeptide (VIP)-expressing interneurons, in auditory cortex that is recruited by behavioral reinforcers and mediates disinhibitory control by inhibiting other inhibitory neurons. As the same disinhibitory cortical circuit is present virtually throughout cortex, we wondered whether VIP neurons are likewise recruited by reinforcers throughout cortex. We monitored VIP neural activity in dozens of cortical regions using three-dimensional random access two-photon microscopy and fiber photometry while mice learned an auditory discrimination task. We found that reward and punishment during initial learning produce rapid, cortex-wide activation of most VIP interneurons. This global recruitment mode showed variations in temporal dynamics in individual neurons and across areas. Neither the weak sensory tuning of VIP interneurons in visual cortex nor their arousal state modulation was fully predictive of reinforcer responses. We suggest that the global response mode of cortical VIP interneurons supports a cell-type-specific circuit mechanism by which organism-level information about reinforcers regulates local circuit processing and plasticity.