Direction-selective motion discrimination by traveling waves in visual cortex.

Stewart Heitmann,G Bard Ermentrout,Hugues Berry

doi:10.1371/journal.pcbi.1008164

Stewart Heitmann, G Bard Ermentrout + Show 1 more

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https://doi.org/10.1371/journal.pcbi.1008164

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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.

Highlights

Hubel and Wiesel [1,2,3] laid the theoretical groundwork for the visual system with their discovery that many neurons in the primary visual cortex respond selectively to bars of light that move with a specific direction and speed
It 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
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

Summary

Introduction

Hubel and Wiesel [1,2,3] laid the theoretical groundwork for the visual system with their discovery that many neurons in the primary visual cortex respond selectively to bars of light that move with a specific direction and speed. Such neurons are said to have non-separable spacetime receptive fields (Fig 1A) because their responses to changing patterns of light and dark in the visual field cannot be explained in terms of independent spatial and temporal neural processes [4, 5]. The concept was originally applied to direction-selective cells in the retina [7] and has since been extended to the visual cortex where transmission delays have been posited in the feed-forward projections [8,9,10,11,12,13] and in the lateral connections [14,15,16]

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