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Frequency-specific neural signatures of perceptual content and perceptual stability.

ABSTRACT: 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.

SUBMITTER: Hardstone R

PROVIDER: S-EPMC9550226 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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Frequency-specific neural signatures of perceptual content and perceptual stability.

Hardstone Richard R Flounders Matthew W MW Zhu Michael M He Biyu J BJ

eLife 20220920

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 decod ...[more]

PMID: 36125242

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Project description:The brain uses its intrinsic dynamics to actively predict observed sensory inputs, especially under perceptual ambiguity. However, it remains unclear how this inference process is neurally implemented in biasing perception of ambiguous inputs towards the predicted percepts. The process of perceptual inference can be well illustrated by the phenomenon of bistable apparent motion in the Ternus display, in which subjective perception spontaneously alternates between element motion (EM) and group motion (GM) percepts depending on whether two consecutively presented frames are grouped over time or not. The frequency of alpha-band oscillations has long been hypothesized to gate the temporal window of perceptual grouping over time. Under this hypothesis, variation in the intrinsic alpha frequency should predict perceptual outcome of the bistable Ternus display. Moreover, we hypothesize that the perception system employs this prior knowledge on intrinsic alpha frequency to resolve perceptual ambiguity, by shifting perceptual inference towards the predicted percepts. Using electroencephalography and intracranial recordings, we showed that both between and within subjects, lower prestimulus alpha frequencies (PAFs) predicted the EM percepts since the two frames fell in the same alpha cycle and got temporally integrated, while higher PAFs predicted the GM percepts since the two frames fell in different alpha cycles. Multivariate decoding analysis between the EM percepts with lower PAFs and the GM percepts with higher PAFs further revealed a representation of the subsequently reported bistable percept in the neural signals shortly before the actual appearance of the second frame. Therefore, perceptual inference, based on variation in intrinsic PAFs, biases poststimulus neural representations by inducing preactivation of the predicted percepts. In addition, enhanced prestimulus blood-oxygen-level-dependent (BOLD) signals and network dynamics in the frontoparietal network, together with reduced prestimulus alpha power, upon perceiving the EM percepts suggest that temporal grouping is an attention-demanding process.

Dataset Information

Frequency-specific neural signatures of perceptual content and perceptual stability.

Publications

Frequency-specific neural signatures of perceptual content and perceptual stability.

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