A theory of direction selectivity for macaque primary visual cortex

Abstract

Significance Motion perception is important for primates, and direction selectivity (DS), the ability to perceive the direction a target is moving, is an essential part of motion perception. Yet no satisfactory mechanistic explanation has been proposed for the origin of DS in the primate visual cortex up until now. In this paper, we hypothesize that DS is initiated in feed-forward LGN input as a result of the dynamic differences between the ON and OFF pathways. The mechanisms we propose are biology based, and our theory explains experimental data for all spatial and temporal frequencies in visual stimuli. Exploiting temporal biases in parallel pathways is relevant beyond visual neuroscience; similar ideas likely apply to other types of neural signal processing. This paper offers a theory for the origin of direction selectivity (DS) in the macaque primary visual cortex, V1. DS is essential for the perception of motion and control of pursuit eye movements. In the macaque visual pathway, neurons with DS first appear in V1, in the Simple cell population of the Magnocellular input layer 4Cα. The lateral geniculate nucleus (LGN) cells that project to these cortical neurons, however, are not direction selective. We hypothesize that DS is initiated in feed-forward LGN input, in the summed responses of LGN cells afferent to a cortical cell, and it is achieved through the interplay of 1) different visual response dynamics of ON and OFF LGN cells and 2) the wiring of ON and OFF LGN neurons to cortex. We identify specific temporal differences in the ON/OFF pathways that, together with item 2, produce distinct response time courses in separated subregions; analysis and simulations confirm the efficacy of the mechanisms proposed. To constrain the theory, we present data on Simple cells in layer 4Cα in response to drifting gratings. About half of the cells were found to have high DS, and the DS was broadband in spatial and temporal frequency (SF and TF). The proposed theory includes a complete analysis of how stimulus features such as SF and TF interact with ON/OFF dynamics and LGN-to-cortex wiring to determine the preferred direction and magnitude of DS.