Neural Signatures of Auditory Perceptual Bistability Revealed by Large-Scale Human Intracranial Recordings

Abstract

A key challenge in neuroscience is understanding how sensory stimuli give rise to perception, especially when the process is supported by neural activity from an extended network of brain areas. Perception is inherently subjective, so interrogating its neural signatures requires, ideally, a combination of three factors: (1) behavioral tasks that separate stimulus-driven activity from perception per se; (2) human subjects who self-report their percepts while performing those tasks; and (3) concurrent neural recordings acquired at high spatial and temporal resolution. In this study, we analyzed human electrocorticographic recordings obtained during an auditory task which supported mutually exclusive perceptual interpretations. Eight neurosurgical patients (5 male; 3 female) listened to sequences of repeated triplets where tones were separated in frequency by several semitones. Subjects reported spontaneous alternations between two auditory perceptual states, 1-stream and 2-stream, by pressing a button. We compared averaged auditory evoked potentials (AEPs) associated with 1-stream and 2-stream percepts and identified significant differences between them in primary and nonprimary auditory cortex, surrounding auditory-related temporoparietal cortex, and frontal areas. We developed classifiers to identify spatial maps of percept-related differences in the AEP, corroborating findings from statistical analysis. We used one-dimensional embedding spaces to perform the group-level analysis. Our data illustrate exemplar high temporal resolution AEP waveforms in auditory core region; explain inconsistencies in perceptual effects within auditory cortex, reported across noninvasive studies of streaming of triplets; show percept-related changes in frontoparietal areas previously highlighted by studies that focused on perceptual transitions; and demonstrate that auditory cortex encodes maintenance of percepts and switches between them. SIGNIFICANCE STATEMENT The human brain has the remarkable ability to discern complex and ambiguous stimuli from the external world by parsing mixed inputs into interpretable segments. However, one's perception can deviate from objective reality. But how do perceptual discrepancies occur? What are their anatomical substrates? To address these questions, we performed intracranial recordings in neurosurgical patients as they reported their perception of sounds associated with two mutually exclusive interpretations. We identified signatures of subjective percepts as distinct from sound-driven brain activity in core and non-core auditory cortex and frontoparietal cortex. These findings were compared with previous studies of auditory bistable perception and suggested that perceptual transitions and maintenance of perceptual states were supported by common neural substrates.

Voluntary auditory change: First-person access to agentive aspects of attention regulation

“…Here, the ambiguity of perceptual interpretations, related to one and the same physical stimulus, allows the observer to consciously influence what is perceived, at least to some extent. In recent experimental studies, however, the role of conscious attention is mostly restricted to a binary decision by the subjects (via button press) which one of two possible percepts is perceived with a prescribed perceptual intention, equally for vision (Kornmeier et al, 2009;van Ee et al, 2005) and audition (Alain et al, 2001;Curtu et al, 2019). Then, conscious attention is only deployed to confirm a resultant percept with an appropriate content, regardless of foregoing aspects of attentional processing.…”

Buildup and bistability in auditory streaming as an evidence accumulation process with saturation

“…Stimulus sequences of interleaved A and B pure tones have been widely used in studying segregation of distinct objects in an auditory scene (auditory streaming), in human psychophysics [1][2][3][4][5][6], invasive neurophysiology [1,3,7,8], or in experiments implementing both [9]. A valued stimulus is triplet-streaming ABA − with the tone frequency difference, DF, as a tunable parameter [10]; Fig 1. For small DF human listeners most likely perceive integration (one galloping rhythm); for DF large, segregation dominates (two simultaneously heard parallel streams).…”

“…Stimulus sequences of interleaved A and B pure tones have been widely used in studying segregation of distinct objects in an auditory scene (auditory streaming), in human psychophysics [ 1 – 6 ], invasive neurophysiology [ 1 , 3 , 7 , 8 ], or in experiments implementing both [ 9 ]. A valued stimulus is triplet-streaming ABA − with the tone frequency difference, DF , as a tunable parameter [ 10 ]; Fig 1 .…”

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.…”