Bistable Perception Modeled as Competing Stochastic Integrations at Two Levels

We propose a novel explanation for bistable perception, namely, the collective dynamics of multiple neural populations that are individually meta-stable. Distributed representations of sensory input and of perceptual state build gradually through noise-driven transitions in these populations, until the competition between alternative representations is resolved by a threshold mechanism. The perpetual repetition of this collective race to threshold renders perception bistable. This collective dynamics – which is largely uncoupled from the time-scales that govern individual populations or neurons – explains many hitherto puzzling observations about bistable perception: the wide range of mean alternation rates exhibited by bistable phenomena, the consistent variability of successive dominance periods, and the stabilizing effect of past perceptual states. It also predicts a number of previously unsuspected relationships between observable quantities characterizing bistable perception. We conclude that bistable perception reflects the collective nature of neural decision making rather than properties of individual populations or neurons.Author Summary: The instability of perception is one of the oldest puzzles in neuroscience. When visual stimulation is even slightly ambiguous, perceptual experience fails to stabilize and alternates perpetually between distinct states. The details of this ‘bistable perception’ have been studied extensively for decades. Here we propose that bistable perception reflects the stochastic integration over many meta-stable populations at two levels of neural representation. While previous accounts of bistable perception rely on an oscillatory dynamic, our model is inherently stochastic. We argue that a fluctuation-driven process accounts naturally for key characteristics of bistable perception that have remained puzzling for decades. For example, our model is the first to explain why the statistical variability of successive dominance periods remains essentially the same, while the mean alternation rates of bistable phenomena range over two orders of magnitude. By postulating two levels of representation that are driven by stimulation and by perceptual state, respectively, our model further accounts for the stabilizing influence of past perceptual states, which are particularly evident in intermittent displays. In general, a fluctuation-driven process decouples the collective dynamics of bistable perception from single-neuron properties and predicts a number of hitherto unsuspected relations between behaviorally observable measures.