Perceptual memory drives learning of retinotopic biases for bistable stimuli

Aidan P. Murphy, David A. Leopold, Andrew E. Welchman

The visual system exploits past experience at multiple timescales to resolve perceptual ambiguity in the retinal image. For example, perception of a bistable stimulus can be biased toward one interpretation over another when preceded by a brief presentation of a disambiguated version of the stimulus (positive priming) or through intermittent presentations of the ambiguous stimulus (stabilization). Similarly, prior presentations of unambiguous stimuli can be used to explicitly "train" a long-lasting association between a percept and a retinal location (perceptual association). These phenonema have typically been regarded as independent processes, with short-term biases attributed to perceptual memory and longer-term biases described as associative learning. Here we tested for interactions between these two forms of experience-dependent perceptual bias and demonstrate that short-term processes strongly influence long-term outcomes. We first demonstrate that the establishment of long-term perceptual contingencies does not require explicit training by unambiguous stimuli, but can arise spontaneously during the periodic presentation of brief, ambiguous stimuli. Using rotating Necker cube stimuli, we observed enduring, retinotopically specific perceptual biases that were expressed from the outset and remained stable for up to 40 min, consistent with the known phenomenon of perceptual stabilization. Further, bias was undiminished after a break period of 5 min, but was readily reset by interposed periods of continuous, as opposed to periodic, ambiguous presentation. Taken together, the results demonstrate that perceptual biases can arise naturally and may principally reflect the brain's tendency to favor recent perceptual interpretation at a given retinal location. Further, they suggest that an association between retinal location and perceptual state, rather than a physical stimulus, is sufficient to generate long-term biases in perceptual organization.