Direction-selective motion discrimination by traveling waves in visual cortex

Abstract

The majority of neurons in primary visual cortex respond selectively to bars of light that have a specific orientation and move in a specific direction. The spatial and temporal responses of such neurons are non-separable. How neurons accomplish that computational feat without resort to explicit time delays is unknown. We propose a novel neural mechanism whereby visual cortex computes non-separable responses by generating endogenous traveling waves of neural activity that resonate with the space-time signature of the visual stimulus. The spatiotemporal characteristics of the response are defined by the local topology of excitatory and inhibitory lateral connections in the cortex. We simulated the interaction between endogenous traveling waves and the visual stimulus using spatially distributed populations of excitatory and inhibitory neurons with Wilson-Cowan dynamics and inhibitory-surround coupling. Our model reliably detected visual gratings that moved with a given speed and direction provided that we incorporated neural competition to suppress false motion signals in the opposite direction. The findings suggest that endogenous traveling waves in visual cortex can impart direction-selectivity on neural responses without resort to explicit time delays. They also suggest a functional role for motion opponency in eliminating false motion signals. Author summaryIt is well established that the so-called simple cells of the primary visual cortex respond preferentially to oriented bars of light that move across the visual field with a particular speed and direction. The spatiotemporal responses of such neurons are said to be non-separable because they cannot be constructed from independent spatial and temporal neural mechanisms. Contemporary theories of how neurons compute non-separable responses typically rely on finely tuned transmission delays between signals from disparate regions of the visual field. However the existence of such delays is controversial. We propose an alternative neural mechanism for computing non-separable responses that does not require transmission delays. It instead relies on the predisposition of the cortical tissue to spontaneously generate spatiotemporal waves of neural activity that travel with a particular speed and direction. We propose that the endogenous wave activity resonates with the visual stimulus to elicit direction-selective neural responses to visual motion. We demonstrate the principle in computer models and show that competition between opposing neurons robustly enhances their ability to discriminate between visual gratings that move in opposite directions.