Layered Structure of Cortex Explains Reversal Dynamics in Bistable Perception

Abstract

AbstractBistable perception involves the spontaneous alternation between two exclusive interpretations of a single stimulus. Previous research has suggested that this perceptual phenomenon results from winnerless dynamics in the cortex. Indeed, winnerless dynamics can explain many key behavioral characteristics of bistable perception. However, it fails to explain an increase in alternation rate that is typically observed in response to increased stimulus drive and instead predicts a decline in alternation rate. To reconcile this discrepancy, several lines of work have augmented winnerless dynamics with additional processes such as global gain control, input suppression, and release mechanisms. These offer potential explanations at an algorithmic level. But it remains unclear which, if any, of these mechanisms are implemented in the cortex and what their biological substrates might be. We show that the answers to these questions lie within the architecture of the cortical microcircuit. Utilizing a dynamic mean field approach, we implement a laminar columnar circuit with empirically derived interlaminar connectivity. By coupling two such circuits such that they exhibit competition, we are able to produce winnerless dynamics reflective of bistable perception. Within our model, we identify two mechanisms through which the layered structure of the cortex gives rise to increased alternation rate in response to increased stimulus drive. First, deep layers act to inhibit the upper layers, thereby reducing the attractor depth and increasing the alternation rate. Second, recurrent connections between superficial and granular layers implement an input suppression mechanism which again reduces the attractor depth of the winnerless competition. These findings demonstrate the functional significance of the layered cortical architecture as they showcase perceptual implications of neuroatomical properties such as interlaminar connectivity and layer-specific activation.Author summaryIn our study, we explore the mechanistic underpinnings of bistable perception, a phenomenon where a single visual stimulus can be perceived in two distinct ways, and where our percept alternates spontaneously between interpretations. Although winnerless competition mechanisms have been widely recognized to govern this, they fall short in explaining why we observe more perceptual alternations with a stronger stimulus. To uncover the cortex’s role in this discrepancy, we constructed a detailed model that mirrors the layered structure and interlaminar connections of the cortex. Remarkably, the architecture of these layers emerged as instrumental players. We discovered that the deeper layers of the cortex seem to inhibit the upper layers, facilitating a quicker alternation between perceptions when stimulated. Additionally, the interlaminar recurrent connections between the upper ‘output’ layer and middle ‘input’ layer appeared to destabilize the prevailing interpretation of the stimulus, leading to faster alternations. Our research illuminates how the complex architecture of the cortex, particularly the interconnections between its layers, plays a pivotal role in influencing our perception. The layered structure of the cortex goes beyond mere anatomy; it influences our perceptual experiences.