A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex

• Published in: Neuron (Cambridge, Mass.) Vol. 108; no. 6; pp. 1181 - 1193.e8
• Main Authors: Keller, Andreas J., Dipoppa, Mario, Roth, Morgane M., Caudill, Matthew S., Ingrosso, Alessandro, Miller, Kenneth D., Scanziani, Massimo
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 23.12.2020; Elsevier Limited
• Subjects: Animals; Calcium - metabolism; canonical disinhibitory circuit; computational modeling; Computational neuroscience; contextual modulation; figure-ground segregation; inhibitory neurons; Intestine; Mice; Models, Neurological; Neural Inhibition - physiology; Neurons; Neurons - metabolism; Photic Stimulation; pop-out effects; recurrent neural network; saliency; Somatostatin; Somatostatin - metabolism; stabilized supralinear network; Vasoactive agents; Vasoactive intestinal peptide; Vasoactive Intestinal Peptide - metabolism; Visual cortex; Visual Cortex - metabolism; Visual Cortex - physiology; Visual pathways; Visual Pathways - metabolism; Visual Pathways - physiology; Visual Perception - physiology; Visual stimuli; figure-ground segregation; recurrent neural network; visual cortex; canonical disinhibitory circuit; computational modeling; contextual modulation; pop-out effects; saliency; inhibitory neurons; stabilized supralinear network
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2020.11.013

Context guides perception by influencing stimulus saliency. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The underlying mechanisms remain unclear. Here, we use optical recordings, manipulations, and computational modeling to show that disinhibitory circuits consisting of vasoactive intestinal peptide (VIP)-expressing and somatostatin (SOM)-expressing inhibitory neurons modulate responses in mouse visual cortex depending on similarity between stimulus and surround, primarily by modulating recurrent excitation. When stimulus and surround are similar, VIP neurons are inactive, and activity of SOM neurons leads to suppression of excitatory neurons. However, when stimulus and surround differ, VIP neurons are active, inhibiting SOM neurons, which leads to relief of excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit that contributes to contextual modulation and may regulate perceptual saliency. •Visual context modulates the response of SOM oppositely to all other V1 neurons•The VIP-SOM disinhibitory circuit controls the impact of context on V1 responses•The VIP-SOM disinhibitory circuit controls V1 by modulating recurrent excitation•As we predict by modeling, silencing of VIP neurons reduces contextual modulation Context provides meaning by influencing perception. In the visual world, context is the visual environment surrounding a visual scene. Here, Keller et al. report that a canonical disinhibitory circuit controls the response of mouse visual cortex to a visual stimulus depending on the context within which that stimulus is presented.