skip to main content


Title: 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
NSF-PAR ID:
10411054
Author(s) / Creator(s):
;
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
  1. 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
  2. Introduction:Current brain-computer interfaces (BCIs) primarily rely on visual feedback. However, visual feedback may not be sufficient for applications such as movement restoration, where somatosensory feedback plays a crucial role. For electrocorticography (ECoG)-based BCIs, somatosensory feedback can be elicited by cortical surface electro-stimulation [1]. However, simultaneous cortical stimulation and recording is challenging due to stimulation artifacts. Depending on the orientation of stimulating electrodes, their distance to the recording site, and the stimulation intensity, these artifacts may overwhelm the neural signals of interest and saturate the recording bioamplifiers, making it impossible to recover the underlying information [2]. To understand how these factors affect artifact propagation, we performed a preliminary characterization of ECoG signals during cortical stimulation.Materials/Methods/ResultsECoG electrodes were implanted in a 39-year old epilepsy patient as shown in Fig. 1. Pairs of adjacent electrodes were stimulated as a part of language cortical mapping. For each stimulating pair, a charge-balanced biphasic square pulse train of current at 50 Hz was delivered for five seconds at 2, 4, 6, 8 and 10 mA. ECoG signals were recorded at 512 Hz. The signals were then high-pass filtered (≥1.5 Hz, zero phase), and the 5-second stimulation epochs were segmented. Within each epoch, artifact-induced peaks were detected for each electrode, except the stimulating pair, where signals were clipped due to amplifier saturation. These peaks were phase-locked across electrodes and were 20 ms apart, thus matching the pulse train frequency. The response was characterized by calculating the median peak within the 5-second epochs. Fig. 1 shows a representative response of the right temporal grid (RTG), with the stimulation channel at RTG electrodes 14 and 15. It also shows a hypothetical amplifier saturation contour of an implantable, bi-directional, ECoG-based BCI prototype [2], assuming the supply voltage of 2.2 V and a gain of 66 dB. Finally, we quantify the worstcase scenario by calculating the largest distance between the saturation contour and the midpoint of each stimulating channel.Discussion:Our results indicate that artifact propagation follows a dipole potential distribution with the extent of the saturation region (the interior of the white contour) proportional to the stimulation amplitude. In general, the artifacts propagated farthest when a 10 mA current was applied with the saturation regions extending from 17 to 32 mm away from the midpoint of the dipole. Consistent with the electric dipole model, this maximum spread happened along the direction of the dipole moment. An exception occurred at stimulation channel RTG11-16, for which an additional saturation contour emerged away from the dipole contour (not shown), extending the saturation region to 41 mm. Also, the worst-case scenario was observed at 6 mA stimulation amplitude. This departure could be a sign of a nonlinear, switch-like behavior, wherein additional conduction pathways could become engaged in response to sufficiently high stimulation.Significance:While ECoG stimulation is routinely performed in the clinical setting, quantitative studies of the resulting signals are lacking. Our preliminary study demonstrates that stimulation artifacts largely obey dipole distributions, suggesting that the dipole model could be used to predict artifact propagation. Further studies are necessary to ascertain whether these results hold across other subjects and combinations of stimulation/recording grids. Once completed, these studies will reveal practical design constraints for future implantable bi-directional ECoG-based BCIs. These include parameters such as the distances between and relative orientations of the stimulating and recording electrodes, the choice of the stimulating electrodes, the optimal placement of the reference electrode, and the maximum stimulation amplitude. These findings would also have important implications for the design of custom, low-power bioamplifiers for implantable bi-directional ECoG-based BCIs.References:[1] Hiremath, S. V., et al. "Human perception of electrical stimulation on the surface of somatosensory cortex." PloS one 12.5 (2017): e0176020.[2] Rouse, A. G., et al. "A chronic generalized bi-directional brain-machine interface." Journal of Neural Engineering 8.3 (2011): 036018 
    more » « less
  3. Advances in artificial intelligence have inspired a paradigm shift in human neuroscience, yielding large-scale functional magnetic resonance imaging (fMRI) datasets that provide high-resolution brain responses to thousands of naturalistic visual stimuli. Because such experiments necessarily involve brief stimulus durations and few repetitions of each stimulus, achieving sufficient signal-to-noise ratio can be a major challenge. We address this challenge by introducing GLMsingle , a scalable, user-friendly toolbox available in MATLAB and Python that enables accurate estimation of single-trial fMRI responses ( glmsingle.org ). Requiring only fMRI time-series data and a design matrix as inputs, GLMsingle integrates three techniques for improving the accuracy of trial-wise general linear model (GLM) beta estimates. First, for each voxel, a custom hemodynamic response function (HRF) is identified from a library of candidate functions. Second, cross-validation is used to derive a set of noise regressors from voxels unrelated to the experiment. Third, to improve the stability of beta estimates for closely spaced trials, betas are regularized on a voxel-wise basis using ridge regression. Applying GLMsingle to the Natural Scenes Dataset and BOLD5000, we find that GLMsingle substantially improves the reliability of beta estimates across visually-responsive cortex in all subjects. Comparable improvements in reliability are also observed in a smaller-scale auditory dataset from the StudyForrest experiment. These improvements translate into tangible benefits for higher-level analyses relevant to systems and cognitive neuroscience. We demonstrate that GLMsingle: (i) helps decorrelate response estimates between trials nearby in time; (ii) enhances representational similarity between subjects within and across datasets; and (iii) boosts one-versus-many decoding of visual stimuli. GLMsingle is a publicly available tool that can significantly improve the quality of past, present, and future neuroimaging datasets sampling brain activity across many experimental conditions. 
    more » « less
  4. Abstract

    The development of the ability to anticipate—as manifested by preparatory actions and neural activation related to the expectation of an upcoming stimulus—may play a key role in the ontogeny of cognitive skills more broadly. This preregistered study examined anticipatory brain potentials and behavioral responses (reaction time; RT) to anticipated target stimuli in relation to individual differences in the ability to use goals to direct action (as indexed by measures of executive function; EF). A cross‐sectional investigation was conducted in 40 adults (aged 18–25 years) and 40 children (aged 6–8 years) to examine the association of changes in the amplitude of modality‐specific alpha‐range rhythms in the electroencephalogram (EEG) during anticipation of lateralized visual, tactile, or auditory stimuli with inter‐ and intraindividual variation in RT and EF. Children and adults exhibited contralateral anticipatory reductions in the mu rhythm and the visual alpha rhythm for tactile and visual anticipation, respectively, indicating modality and spatially specific attention allocation. Variability in within‐subject anticipatory alpha lateralization (the difference between contralateral and ipsilateral alpha power) was related to single‐trial RT. This relation was more prominent in adults than in children, and was not apparent for auditory stimuli. Multilevel models indicated that interindividual differences in anticipatory mu rhythm lateralization contributed to the significant association with variability in EF, but this was not the case for visual or auditory alpha rhythms. Exploratory microstate analyses were undertaken to cluster global field power (GFP) into a distribution‐free temporal analysis examining developmental differences across samples and in relation to RT and EF. Anticipation is suggested as a developmental bridge construct connecting neuroscience, behavior, and cognition, with anticipatory EEG oscillations being discussed as quantifiable and potentially malleable indicators of stimulus prediction.

     
    more » « less
  5. Abstract

    A longstanding debate has surrounded the role of the motor system in speech perception, but progress in this area has been limited by tasks that only examine isolated syllables and conflate decision-making with perception. Using an adaptive task that temporally isolates perception from decision-making, we examined an EEG signature of motor activity (sensorimotor μ/beta suppression) during the perception of auditory phonemes, auditory words, audiovisual words, and environmental sounds while holding difficulty constant at two levels (Easy/Hard). Results revealed left-lateralized sensorimotor μ/beta suppression that was related to perception of speech but not environmental sounds. Audiovisual word and phoneme stimuli showed enhanced left sensorimotor μ/beta suppression for correct relative to incorrect trials, while auditory word stimuli showed enhanced suppression for incorrect trials. Our results demonstrate that motor involvement in perception is left-lateralized, is specific to speech stimuli, and it not simply the result of domain-general processes. These results provide evidence for an interactive network for speech perception in which dorsal stream motor areas are dynamically engaged during the perception of speech depending on the characteristics of the speech signal. Crucially, this motor engagement has different effects on the perceptual outcome depending on the lexicality and modality of the speech stimulus.

     
    more » « less