Distortions in perceived direction of motion predicted by population response dynamics in primary visual cortex

Abstract

Encoding the trajectory of a moving stimulus that abruptly changes its direction of motion provides a particularly vivid example of the challenges inherent in using cortical circuits to represent rapidly changing stimulus features that are ubiquitous in visual scenes. Instantaneous changes in the properties of a visual stimulus are accompanied by changes in the activity of cortical circuits that may outlast the stimulus event by 100's of milliseconds (), but how these complex circuit dynamics impact population coding mechanisms remains unclear. Here we employed in vivo voltage sensitive dye (VSD) imaging to explore how abrupt changes in the trajectory of a moving stimulus impact the population coding of motion direction in ferret primary visual cortex (V1). For motion in a constant direction, the peak of the cortical population response reliably signaled the stimulus trajectory; but for abrupt changes in motion direction, the peak of the population response departed significantly from the stimulus trajectory in a fashion that depended on the size of the direction deviation. For small direction deviation angles, the peak of the active population shifted from values consistent with the initial direction of motion to those consistent with the final direction of motion by progressing smoothly through intermediate directions not present in the stimulus. In contrast, for large direction deviation angles, peak values consistent with the initial motion direction were followed by: a small deviation away from the final motion direction, a rapid 180 degree jump, and a gradual shift to the final direction. While the basic qualities of the population response to motion transitions are consistent with linear summation of the response to each component, direct tests of linearity reveal the presence of additional nonlinear mechanisms that shape the dynamics of population response both during and after motion transitions. These departures of the population response from the actual trajectory of the stimulus predict specific misperceptions of motion direction that were confirmed by human psychophysical experiments. Small angular deviations in direction of motion are perceived as smoother than the actual stimulus change, while large angular deviations are perceived as sharper than the actual stimulus change. We conclude that cortical dynamics and population coding mechanisms combine to place constraints on the accuracy with which abrupt changes in direction of motion can be represented by cortical circuits. The smoothing of small direction deviations and the sharpening of larger deviations could serve to enhance the discrimination of continuous and discontinuous motion trajectories. But even if these perceptual distortions are not beneficial, their existence must represent an acceptable tradeoff that balances the need for accuracy with the innumerable advantages that are afforded by distributed coding mechanisms.