Classical-Contextual Interactions in V1 May Rely on Dendritic Computations

•How object contours are detected in visual cortex remains poorly understood.•Combining cues within and outside the classical RF is thought to be crucial.•We collect the first classical-contextual interaction function from natural images.•Nonlinear synaptic interactions in dendrites could support the CC-IF computation.•Interneuron circuitry increases the flexibility of CC-IF computations. A signature feature of the neocortex is the dense network of horizontal connections (HCs) through which pyramidal neurons (PNs) exchange “contextual” information. In primary visual cortex (V1), HCs are thought to facilitate boundary detection, a crucial operation for object recognition, but how HCs modulate PN responses to boundary cues within their classical receptive fields (CRF) remains unknown. We began by “asking” natural images, through a structured data collection and ground truth labeling process, what function a V1 cell should use to compute boundary probability from aligned edge cues within and outside its CRF. The “answer” was an asymmetric 2-D sigmoidal function, whose nonlinear form provides the first normative account for the “multiplicative” center-flanker interactions previously reported in V1 neurons (Kapadia et al., 1995, 2000; Polat et al., 1998). Using a detailed compartmental model, we then show that this boundary-detecting classical-contextual interaction function can be computed by NMDAR-dependent spatial synaptic interactions within PN dendrites – the site where classical and contextual inputs first converge in the cortex. In additional simulations, we show that local interneuron circuitry activated by HCs can powerfully leverage the nonlinear spatial computing capabilities of PN dendrites, providing the cortex with a highly flexible substrate for integration of classical and contextual information.