Top-down input modulates visual context processing through an interneuron-specific circuit
Georgia Bastos,
Jacob T. Holmes,
Jordan M. Ross,
Anna M. Rader,
Connor G. Gallimore,
Joseph A. Wargo,
Darcy S. Peterka,
Jordan P. Hamm
Affiliations
Georgia Bastos
Neuroscience Institute, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA; Center for Neuroinflammation and Cardiometabolic Diseases, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA
Jacob T. Holmes
Neuroscience Institute, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA
Jordan M. Ross
Neuroscience Institute, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA; Center for Behavioral Neuroscience, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA
Anna M. Rader
Neuroscience Institute, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA; Center for Neuroinflammation and Cardiometabolic Diseases, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA
Connor G. Gallimore
Neuroscience Institute, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA
Joseph A. Wargo
Neuroscience Institute, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA
Darcy S. Peterka
Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA
Jordan P. Hamm
Neuroscience Institute, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA; Center for Neuroinflammation and Cardiometabolic Diseases, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA; Center for Behavioral Neuroscience, Georgia State University, Petit Science Center, 100 Piedmont Ave, Atlanta, GA 30303, USA; Corresponding author
Summary: Visual stimuli that deviate from the current context elicit augmented responses in the primary visual cortex (V1). These heightened responses, known as “deviance detection,” require local inhibition in the V1 and top-down input from the anterior cingulate area (ACa). Here, we investigated the mechanisms by which the ACa and V1 interact to support deviance detection. Local field potential recordings in mice during an oddball paradigm showed that ACa-V1 synchrony peaks in the theta/alpha band (≈10 Hz). Two-photon imaging in the V1 revealed that mainly pyramidal neurons exhibited deviance detection, while contextually redundant stimuli increased vasoactive intestinal peptide (VIP)-positive interneuron (VIP) activity and decreased somatostatin-positive interneuron (SST) activity. Optogenetic drive of ACa-V1 inputs at 10 Hz activated V1-VIPs but inhibited V1-SSTs, mirroring the dynamics present during the oddball paradigm. Chemogenetic inhibition of V1-VIPs disrupted Aca-V1 synchrony and deviance detection in the V1. These results outline temporal and interneuron-specific mechanisms of top-down modulation that support visual context processing.
