An official website of the United States government
Abstract Ambiguous images elicit bistable perception, wherein periods of momentary perceptual stability are interrupted by sudden perceptual switches. When intermittently presented, ambiguous images trigger a perceptual memory trace in the intervening blank periods. Understanding the neural bases of perceptual stability and perceptual memory during bistable perception may hold clues for explaining the apparent stability of visual experience in the natural world, where ambiguous and fleeting images are prevalent. Motivated by recent work showing the involvement of the right inferior frontal gyrus (rIFG) in bistable perception, we conducted a transcranial direct-current stimulation (tDCS) study with a double-blind, within-subject cross-over design to test a potential causal role of rIFG in these processes. Subjects viewed ambiguous images presented continuously or intermittently while under EEG recording. We did not find any significant tDCS effect on perceptual behavior. However, the fluctuations of oscillatory power in the alpha and beta bands predicted perceptual stability, with higher power corresponding to longer percept durations. In addition, higher alpha and beta power predicted enhanced perceptual memory during intermittent viewing. These results reveal a unified neurophysiological mechanism sustaining perceptual stability and perceptual memory when the visual system is faced with ambiguous input.
more »
« less
Attractor-Like Dynamics Extracted from Human Electrocorticographic Recordings Underlie Computational Principles of Auditory Bistable Perception
In bistable perception, observers experience alternations between two interpretations of an unchanging stimulus. Neurophysiological studies of bistable perception typically partition neural measurements into stimulus-based epochs and assess neuronal differences between epochs based on subjects' perceptual reports. Computational studies replicate statistical properties of percept durations with modeling principles like competitive attractors or Bayesian inference. However, bridging neuro-behavioral findings with modeling theory requires the analysis of single-trial dynamic data. Here, we propose an algorithm for extracting nonstationary timeseries features from single-trial electrocorticography (ECoG) data. We applied the proposed algorithm to 5-min ECoG recordings from human primary auditory cortex obtained during perceptual alternations in an auditory triplet streaming task (six subjects: four male, two female). We report two ensembles of emergent neuronal features in all trial blocks. One ensemble consists of periodic functions that encode a stereotypical response to the stimulus. The other comprises more transient features and encodes dynamics associated with bistable perception at multiple time scales: minutes (within-trial alternations), seconds (duration of individual percepts), and milliseconds (switches between percepts). Within the second ensemble, we identified a slowly drifting rhythm that correlates with the perceptual states and several oscillators with phase shifts near perceptual switches. Projections of single-trial ECoG data onto these features establish low-dimensional attractor-like geometric structures invariant across subjects and stimulus types. These findings provide supporting neural evidence for computational models with oscillatory-driven attractor-based principles. The feature extraction techniques described here generalize across recording modality and are appropriate when hypothesized low-dimensional dynamics characterize an underlying neural system. SIGNIFICANCE STATEMENTIrrespective of the sensory modality, neurophysiological studies of multistable perception have typically investigated events time-locked to the perceptual switching rather than the time course of the perceptual states per se. Here, we propose an algorithm that extracts neuronal features of bistable auditory perception from largescale single-trial data while remaining agnostic to the subject's perceptual reports. The algorithm captures the dynamics of perception at multiple timescales, minutes (within-trial alternations), seconds (durations of individual percepts), and milliseconds (timing of switches), and distinguishes attributes of neural encoding of the stimulus from those encoding the perceptual states. Finally, our analysis identifies a set of latent variables that exhibit alternating dynamics along a low-dimensional manifold, similar to trajectories in attractor-based models for perceptual bistability.
more »
« less
- Award ID(s):
- 1840260
- PAR ID:
- 10411054
- Publisher / Repository:
- DOI PREFIX: 10.1523
- Date Published:
- Journal Name:
- The Journal of Neuroscience
- Volume:
- 43
- Issue:
- 18
- ISSN:
- 0270-6474
- Page Range / eLocation ID:
- p. 3294-3311
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Perception can be highly dependent on stimulus context, but whether and how sensory areas encode the context remains uncertain. We used an ambiguous auditory stimulus – a tritone pair – to investigate the neural activity associated with a preceding contextual stimulus that strongly influenced the tritone pair’s perception: either as an ascending or a descending step in pitch. We recorded single-unit responses from a population of auditory cortical cells in awake ferrets listening to the tritone pairs preceded by the contextual stimulus. We find that the responses adapt locally to the contextual stimulus, consistent with human MEG recordings from the auditory cortex under the same conditions. Decoding the population responses demonstrates that cells responding to pitch-changes are able to predict well the context-sensitive percept of the tritone pairs. Conversely, decoding the individual pitch representations and taking their distance in the circular Shepard tone space predicts theoppositeof the percept. The various percepts can be readily captured and explained by a neural model of cortical activity based on populations of adapting, pitch and pitch-direction cells, aligned with the neurophysiological responses. Together, these decoding and model results suggest that contextual influences on perception may well be already encoded at the level of the primary sensory cortices, reflecting basic neural response properties commonly found in these areas.more » « less
-
Performance during perceptual decision-making exhibits an inverted-U relationship with arousal, but the underlying network mechanisms remain unclear. Here, we recorded from auditory cortex (A1) of behaving mice during passive tone presentation, while tracking arousal via pupillometry. We found that tone discriminability in A1 ensembles was optimal at intermediate arousal, revealing a population-level neural correlate of the inverted-U relationship. We explained this arousal-dependent coding using a spiking network model with a clustered architecture. Specifically, we show that optimal stimulus discriminability is achieved near a transition between a multi-attractor phase with metastable cluster dynamics (low arousal) and a single-attractor phase (high arousal). Additional signatures of this transition include arousal-induced reductions of overall neural variability and the extent of stimulus-induced variability quenching, which we observed in the empirical data. Our results elucidate computational principles underlying interactions between pupil-linked arousal, sensory processing, and neural variability, and suggest a role for phase transitions in explaining nonlinear modulations of cortical computations.more » « less
-
null (Ed.)Abstract Information processing under conditions of uncertainty requires the involvement of cognitive control. Despite behavioral evidence of the supramodal function (i.e., independent of sensory modality) of cognitive control, the underlying neural mechanism needs to be directly tested. This study used functional magnetic imaging together with visual and auditory perceptual decision-making tasks to examine brain activation as a function of uncertainty in the two stimulus modalities. The results revealed a monotonic increase in activation in the cortical regions of the cognitive control network (CCN) as a function of uncertainty in the visual and auditory modalities. The intrinsic connectivity between the CCN and sensory regions was similar for the visual and auditory modalities. Furthermore, multivariate patterns of activation in the CCN predicted the level of uncertainty within and across stimulus modalities. These findings suggest that the CCN implements cognitive control by processing uncertainty as abstract information independent of stimulus modality.more » « less
-
In the natural environment, we often form stable perceptual experiences from ambiguous and fleeting sensory inputs. Which neural activity underlies the content of perception and which neural activity supports perceptual stability remains an open question. We used a bistable perception paradigm involving ambiguous images to behaviorally dissociate perceptual content from perceptual stability, and magnetoencephalography to measure whole-brain neural dynamics in humans. Combining multivariate decoding and neural state-space analyses, we found frequency-band-specific neural signatures that underlie the content of perception and promote perceptual stability, respectively. Across different types of images, non-oscillatory neural activity in the slow cortical potential (<5 Hz) range supported the content of perception. Perceptual stability was additionally influenced by the amplitude of alpha and beta oscillations. In addition, neural activity underlying perceptual memory, which supports perceptual stability when sensory input is temporally removed from view, also encodes elapsed time. Together, these results reveal distinct neural mechanisms that support the content versus stability of visual perception.more » « less
