Top-down input modulates visual context processing through an interneuron-specific circuit

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. [Display omitted] •Visual cortex processes stimuli in context, detecting deviant stimuli in predictable sequences•Prefrontal and visual cortex synchronize at ≈10 Hz during predictable sequences•Subsets of VIP neurons increase and SSTs decrease activity during predictable sequences•Inactivation of VIPs disrupts 10-Hz fronto-visual synchrony and visual context processing Bastos et al. studied how the brain processes visual stimuli in context. They find that a prefrontal region, the ACa, modulates the visual cortex, sending spatiotemporal patterns of activity that correlate with stimulus predictability. This engages a VIP-SST interneuronal circuit in the visual cortex to indirectly bolster responses to contextually deviant stimuli.