Ensemble modeling of auditory streaming reveals potential sources of bistability across the perceptual hierarchy

Abstract

<jats:title>Abstract</jats:title><jats:p>Perceptual bistability—the spontaneous fluctuation of perception between two interpretations of a stimulus—occurs when observing a large variety of ambiguous stimulus configurations. This phenomenon has the potential to serve as a tool for, among other things, understanding how function varies across individuals due to the large individual differences that manifest during perceptual bistability. Yet it remains difficult to interpret the functional processes at work, without knowing where bistability arises during perception. In this study we explore the hypothesis that bistability originates from multiple sources distributed across the perceptual hierarchy. We develop a hierarchical model of auditory processing comprised of three distinct levels: a Peripheral, tonotopic analysis, a Central analysis computing features found more centrally in the auditory system, and an Object analysis, where sounds are segmented into different streams. We model bistable perception within this system by injecting adaptation, inhibition and noise into one or all of the three levels of the hierarchy. We evaluate a large ensemble of variations of this hierarchical model, where each model has a different configuration of adaptation, inhibition and noise. This approach avoids the assumption that a single configuration must be invoked to explain the data. Each model is evaluated based on its ability to replicate two hallmarks of bistability during auditory streaming: the selectivity of bistability to specific stimulus configurations, and the characteristic log-normal pattern of perceptual switches. Consistent with a distributed origin, a broad range of model parameters across this hierarchy lead to a plausible form of perceptual bistability. The ensemble also appears to predict that greater individual variation in adaptation and inhibition occurs in later stages of perceptual processing.</jats:p><jats:sec><jats:title>Author summary</jats:title><jats:p>Our ability to experience the everyday world through our senses requires that we resolve numerous ambiguities present in the physical evidence available. This is accomplished, in part, through a series of hierarchical computations, in which stimulus interpretations grow increasingly abstract. Our ability to resolve ambiguity does not always succeed, such as during optical illusions. In this study, we examine a form of perceptual ambiguity called bistability—cases in which a single individual’s perception spontaneously switches back and forth between two interpretations of a single stimulus. A challenge in understanding bistability is that we don’t know where along the perceptual hierarchy it is generated. Here we test the idea that there are multiple origins by building a simulation of the auditory system. Consistent with a multi-source account of bistability, this simulation accurately predicts perception of a simple auditory stimulus when bistability originates from a number of different sources within the model. The data also indicate that individual differences during ambiguous perception may primarily originate from higher levels of the perceptual hierarchy. This result provides a clue for future work aiming to determine how auditory function differs across individual brains.</jats:p></jats:sec>

Adaptation in the sensory cortex drives bistable switching during auditory stream segregation

“…Finally, we found similar neural dynamics of adaptation in multiple parts of the superior temporal lobe, including HG, posterior STG, and anterior STG. This is consistent with our computational model ( Little et al. 2020 ), as well as a prior conceptual model ( Tong et al.…”

“…Separate from these possible explanations, it has been widely speculated in the framework of perceptual rivalry that when perception switches, there is release from inhibition of one percept combined with strengthening of the other percept ( Shpiro et al. 2009 ; Little et al. 2020 ).…”

“…The current study further tests the general framework of adaptation, inhibition, and noise—and the specific computational model presented in Little et al. (2020) —using fMRI.…”

“…Two recent papers from our groups provide valuable context for the present study. We published a new computational model that embodies the general mechanisms of adaptation, inhibition, and noise described earlier and applies it to the auditory system ( Little et al. 2020 ).…”