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

Abstract

Perceptual bistability-the spontaneous, irregular 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 applying 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.

Adaptation in sensory cortex drives bistable switching during auditory stream segregation

“…This pattern of dynamic activity in auditory cortex is consistent with our previous finding that the auditory sustained potential was larger following a switch compared to no-switch trials (Higgins et al, 2020), although that study did not track the time course of change like in the current study. Our findings of neural adaptation are also consistent with standard models that explain switches in perception as the result of neural adaptation that destabilizes dominance of the current percept, allowing an alternative percept to gradually overcome inhibition and take over as a new dominant percept (Brascamp et al, 2008;Grossberg et al, 2008;Li et al, 2017;Little et al, 2020;Noest et al, 2007;Rankin et al, 2017;Rankin & Rinzel, 2019;Rankin et al, 2015;Tong et al, 2006;H. R. Wilson, 2003).…”

Resetting of Auditory and Visual Segregation Occurs After Transient Stimuli of the Same Modality

“…Binocular rivalry studies in the visual system indicate that bistable perception is due to neural competition at multiple levels of the visual pathway, including the lateral geniculate nucleus, primary visual cortex, and the ventral pathway of the visual system (Leopold and Logothetis, 1996;Tong, 2001;Blake and Logothetis, 2002;Wunderlich et al, 2005). Support for the ventral pathway as a locus for stream segregation has also been observed in the auditory system (Curtu et al, 2019;Higgins et al, 2020), and this conclusion is further supported by computational modeling that most accurately describes bistable perception as the result of competing levels of adaptation, inhibition, and noise across three levels of hierarchical processing (Little et al, 2020). The resulting hypothesis is that segregation emerges to varying degrees of the ascending sensory system, and is most prominent at later levels of the ventral pathway.…”

“…These perceptual decisions when given ambiguous information require time to build up, after which a percept can be maintained, or superseded by an alternate percept, akin to a balancing act between perceptual stability and sensitivity to newer, more relevant information (Snyder et al, 2015 ). The underlying neural substrate for this bistable process is a combination of adaptation, inhibition, and noise in the sensory pathway, all exerting influence on neural representations of alternating percepts (Rankin et al, 2015 ; Little et al, 2020 ).…”

Resetting of auditory and visual segregation occurs after transient stimuli of the same modality

“…Binocular rivalry studies in the visual system indicate that bistable perception is due to neural competition at multiple levels of the visual pathway, including the lateral geniculate nucleus, primary visual cortex, and the ventral pathway of the visual system (Blake & Logothetis, 2002;Leopold & Logothetis, 1996;Tong, 2001;Wunderlich et al, 2005). Support for the ventral pathway as a locus for stream segregation has also been observed in the auditory system (Curtu et al, 2019;Higgins et al, 2020), and this conclusion is further supported by computational modeling that most accurately describes bistable perception as the result of competing levels of adaptation, inhibition, and noise across three levels of hierarchical processing (Little et al, 2020). The resulting hypothesis is that segregation emerges to varying degrees of the ascending sensory system, and is most prominent at later levels of the ventral pathway.…”

“…These perceptual decisions when given ambiguous information require time to build up, after which a percept can be maintained, or superseded by an alternate percept, akin to a balancing act between perceptual stability and sensitivity to newer, more relevant information (Snyder et al, 2015). The underlying neural substrate for this bistable process is a combination of adaptation, inhibition, and noise in the sensory pathway, all exerting influence on neural representations of alternating percepts (Little et al, 2020).…”