Sharper orientation tuning of the extraclassical suppressive-surround due to a neuron's location in the V1 orientation map emerges late in time

Abstract

Neuronal responses in primary visual cortex (V1) can be suppressed by a stimulus presented to the extraclassical surround, and such interactions are thought to be critical for figure ground segregation and form perception. While surround suppression likely originates from both feedforward afferents and multiple cortical circuits, it is unclear what role each circuit plays in the surround's orientation tuning. To investigate this we recorded from single units in V1 of anesthetized cat and analyzed the orientation tuning of the suppressive-surround over time. In addition, based on orientation maps derived through optical imaging prior to recording, neurons were classified as being located in domains or pinwheels. For both types of neurons, shortly after response onset (10 ms) the suppressive-surround is broadly tuned to orientation, but this is followed by a steep improvement in tuning over the next ∼30 ms. While the tuning of the pinwheel cells plateaus at this point, tuning is enhanced further for domain cells, especially those located superficially in the cortex, reaching a peak at 80 ms from response onset. This relatively slow evolution of the orientation tuning of the suppressive surround suggests that fast-arriving feedforward circuits (10 ms) likely only provide broadly tuned suppression, but that feedback from higher visual areas which is likely to arrive over the next 30 ms and can cover both the receptive field center and the extraclassical surround contributes to the initial steep rise in tuning for both cell types. Moreover, we speculate that the even later enhancement in tuning for domain neurons could mean the involvement of inputs from relatively long-range lateral connections, which not only propagate slowly but also link like-oriented domains corresponding to the receptive field of only the extraclassical surround.