Neural correlates of perceptual switching while listening to bistable auditory streaming stimuli

Higgins, Nathan C.; Little, David; Yerkes, Breanne D.; Nave, Karli; Kuruvilla-Mathew, Abin; Elhilali, Mounya; Snyder, Joel S.

doi:10.1016/j.neuroimage.2019.116220

Cited by 12 publications

(16 citation statements)

References 64 publications

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“…Behavioral Response Patterns. Participant response patterns were consistent with those observed previously using a similar intermittent response paradigm (Higgins et al, 2020). Perceptual responses at the beginning of trials were typically integrated, but average data across uninterrupted segments of the 38 trials within a segment converged towards roughly equal probability of integrated versus segregated perception (Fig.…”

Section: Resultssupporting

confidence: 87%

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Adaptation in sensory cortex drives bistable switching during auditory stream segregation

Higgins¹,

Scurry²,

Jiang³

et al. 2022

Preprint

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The mechanisms of conscious perception have been studied for many years using bistable visual stimuli, which result in switches of perceptual interpretation during viewing, despite a lack of physical change in the stimulus characteristics. Theoretical studies have identified potential neural mechanisms such as neural adaptation, inhibitory competition, and noise, as key components that lead to switches in perception, while neurophysiological studies have identified brain responses and brain areas that appear to be critical to switches in perception. Compared to vision, bistable perception in other modalities is less well understood, although studies on bistable auditory perception performed thus far indicate more similarities than differences with visual bistable perception. We used functional magnetic resonance imaging to study brain activity around the time of switches in perception while participants were listening to a bistable auditory stream segregation stimulus, which can be heard as one integrated stream of pure tones or two segregated streams of tones. The auditory thalamus showed more activity around the time of a switch from segregated to integrated compared to stable perception of integrated; in contrast, the rostral-anterior cingulate cortex and the inferior parietal lobule showed more activity around the time of a switch from integrated to segregated compared to time periods of stable perception of segregated streams, consistent with prior findings of asymmetries in brain activity depending on switch direction. In sound-responsive areas in the auditory cortex, neural activity declined in strength over time following switches in perception, but increased in strength preceding switches in perception. Such dynamics in auditory cortex are consistent with the role of adaptation proposed by computational models of visual and auditory bistable switching, whereby the strength of neural activity decreases in strength following a switch in perception, which eventually destabilizes the current percept enough to lead to a switch to an alternative percept.

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Section: Resultssupporting

confidence: 87%

“…Dipole modeling showed that the sustained response also had a small parietal source, in addition to the main ventral auditory cortex source. We also found this response to be enhanced following switches from one percept to the other (Higgins et al, 2020). This latter finding is consistent with the role of neural adaptation.…”

Section: Introductionsupporting

confidence: 88%

Adaptation in sensory cortex drives bistable switching during auditory stream segregation

Higgins¹,

Scurry²,

Jiang³

et al. 2022

Preprint

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show abstract

“…When relating the pupillometry effects observed here to other psychophysiological measures associated with perceptual multistability, it is important to distinguish between studies that identify physiological correlates of specific percepts (for example with fMRI in visual multistability [59]) from studies that address correlates of the switching process itself. In auditory multistability, correlates of switching have been studied with EEG by Higgins and colleagues [60] and with fMRI by Kashino and Kondo [61]. In visual multistability, switching has been examined with fMRI [14][15][16]62], MEG [63] and EEG [64,65].…”

Section: Plos Onementioning

confidence: 99%

Pupillometry in auditory multistability

et al. 2021

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In multistability, a constant stimulus induces alternating perceptual interpretations. For many forms of visual multistability, the transition from one interpretation to another (“perceptual switch”) is accompanied by a dilation of the pupil. Here we ask whether the same holds for auditory multistability, specifically auditory streaming. Two tones were played in alternation, yielding four distinct interpretations: the tones can be perceived as one integrated percept (single sound source), or as segregated with either tone or both tones in the foreground. We found that the pupil dilates significantly around the time a perceptual switch is reported (“multistable condition”). When participants instead responded to actual stimulus changes that closely mimicked the multistable perceptual experience (“replay condition”), the pupil dilated more around such responses than in multistability. This still held when data were corrected for the pupil response to the stimulus change as such. Hence, active responses to an exogeneous stimulus change trigger a stronger or temporally more confined pupil dilation than responses to an endogenous perceptual switch. In another condition, participants randomly pressed the buttons used for reporting multistability. In Study 1, this “random condition” failed to sufficiently mimic the temporal pattern of multistability. By adapting the instructions, in Study 2 we obtained a response pattern more similar to the multistable condition. In this case, the pupil dilated significantly around the random button presses. Albeit numerically smaller, this pupil response was not significantly different from the multistable condition. While there are several possible explanations–related, e.g., to the decision to respond–this underlines the difficulty to isolate a purely perceptual effect in multistability. Our data extend previous findings from visual to auditory multistability. They highlight methodological challenges in interpreting such data and suggest possible approaches to meet them, including a novel stimulus to simulate the experience of perceptual switches in auditory streaming.

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“…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.…”

Section: Discussionmentioning

confidence: 94%

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

et al. 2021

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In the presence of a continually changing sensory environment, maintaining stable but flexible awareness is paramount, and requires continual organization of information. Determining which stimulus features belong together, and which are separate is therefore one of the primary tasks of the sensory systems. Unknown is whether there is a global or sensory-specific mechanism that regulates the final perceptual outcome of this streaming process. To test the extent of modality independence in perceptual control, an auditory streaming experiment, and a visual moving-plaid experiment were performed. Both were designed to evoke alternating perception of an integrated or segregated percept. In both experiments, transient auditory and visual distractor stimuli were presented in separate blocks, such that the distractors did not overlap in frequency or space with the streaming or plaid stimuli, respectively, thus preventing peripheral interference. When a distractor was presented in the opposite modality as the bistable stimulus (visual distractors during auditory streaming or auditory distractors during visual streaming), the probability of percept switching was not significantly different than when no distractor was presented. Conversely, significant differences in switch probability were observed following within-modality distractors, but only when the pre-distractor percept was segregated. Due to the modality-specificity of the distractor-induced resetting, the results suggest that conscious perception is at least partially controlled by modality-specific processing. The fact that the distractors did not have peripheral overlap with the bistable stimuli indicates that the perceptual reset is due to interference at a locus in which stimuli of different frequencies and spatial locations are integrated.

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Neural correlates of perceptual switching while listening to bistable auditory streaming stimuli

Cited by 12 publications

References 64 publications

Adaptation in sensory cortex drives bistable switching during auditory stream segregation

Adaptation in sensory cortex drives bistable switching during auditory stream segregation

Pupillometry in auditory multistability

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

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