Anticipatory responses along motion trajectories in awake monkey area V1

What are the neural mechanisms underlying motion integration of translating objects? Visual motion integration is generally conceived of as a feedforward, hierarchical, information processing. However, feedforward models fail to account for many contextual effects revealed using natural moving stimuli. In particular, a translating object evokes a sequence of transient feedforward responses in the primary visual cortex but also propagations of activity through horizontal and feedback pathways. We investigated how these pathways shape the representation of a translating bar in monkey V1. We show that, for long trajectories, spiking activity builds-up hundreds of milliseconds before the bar enters the neurons’ receptive fields. Using VSDI and LFP recordings guided by a phenomenological model of propagation dynamics, we demonstrate that this anticipatory response arises from the interplay between horizontal and feedback networks driving V1 neurons well ahead of their feedforward inputs. This mechanism could subtend several perceptual contextual effects observed with translating objects. Highlights Our hypothesis is that lateral propagation of activity in V1 contributes to the integration of translating stimuli Consistent with this hypothesis, we find that a translating bar induces anticipatory spiking activity in V1 neurons. A V1 model describes how this anticipation can arise from inter and intra-cortical lateral propagation of activity. The dynamic of VSDi and LFP signals in V1 is consistent with the predictions made by the model. The intra-cortical origin is further confirmed by the fact that a bar moving from the ipsilateral hemifield does not evoke anticipation. Horizontal and feedback input are not only modulatory but can also drive spiking responses in specific contexts.