Attractor-Like Dynamics Extracted from Human Electrocorticographic Recordings Underlie Computational Principles of Auditory Bistable Perception

Abstract

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 non-stationary timeseries features from single-trial electrocorticography (ECoG) data. We applied the proposed algorithm to 5-minute ECoG recordings from human primary auditory cortex obtained during perceptual alternations in an auditory triplet streaming task (six subjects: 4 male, 2 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 multi-stable 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.

Play it by Ear: A perceptual algorithm for autonomous melodious piano playing with a bio-inspired robotic hand

“…This limited repertoire of experience, as in biology, naturally limits how the melodies were perceived and interpreted (i.e., heard and reproduced, respectively). This perceptual limitation of the PL algorithm is analogous to biological discretization of human hearing—whereby the perceptual field is not continuous, but rather a collection of attractors around the phonemes common in a mother tongue (57; 58). Thus, some spoken accents in a second language cannot be improved upon as the speaker simply cannot distinguish phonemes in the second language that fall into nearby attractors in the mother tongue.…”