Orientation change detection and orientation pooling in space and time performed by two subpopulations of neurons in V2

Abstract

Neurons in V1 mainly extract oriented luminance boundaries, while neurons in V2 detect more complex boundaries, including texture boundaries. Here we investigate the processing of orientation signals in V1 and V2, and find two distinct subpopulations of neurons in V2 based on their dynamics. We recorded responses from single neurons in V1 and V2 of anesthetized monkeys. Stimuli consisted of a 4x5 or 6x6 grid of adjacent rectangular regions, covering the non-classical receptive field. Each region contained sinusoidal gratings with either the preferred orientation or the non-preferred orthogonal orientation controlled by m-sequences (frame rate 20 ms or 40 ms). V1 neurons have monophasic responses to the orientation signal in individual regions, and their timing is consistent across the population. In contrast, V2 neurons have two distinct patterns of responses: some are biphasic, with an initial peak width narrower than the V1 responses (‘transient V2 neurons’); others are monophasic, with a broader peak than the V1 responses (‘sustained V2 neurons’). The biphasic response pattern indicates dynamic orientation tuning and predicts that the optimal stimulus within a patch is the non-preferred orientation followed by the preferred orientation. Responses to combinations of orientations reveal additional distinctions between V1 and the two V2 subpopulations. Neurons in V1 have nonlinear interactions consistent with cross-orientation suppression. Transient V2 neurons exhibit the opposite: larger responses to orientation discontinuities than to continuous orientation. Sustained V2 neurons show no measurable nonlinear spatial interaction. This study shows, firstly, how non-linear as well as linear responses of V2 neurons differ from V1 responses. Secondly, we identified two different classes of orientation selective V2 neurons. The transient V2 neurons differentiate the V1 input in space and time and therefore respond well to changes in orientation. Sustained V2 neurons pool the V1 input and respond better to constant orientation signals.