Vestibular and active self-motion signals drive visual perception in binocular rivalry.
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ABSTRACT:
SUBMITTER: Alais D
PROVIDER: S-EPMC8632839 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The perception of self-motion direction, or heading, relies on integration of multiple sensory cues, especially from the visual and vestibular systems. However, the reliability of sensory information can vary rapidly and unpredictably, and it remains unclear how the brain integrates multiple sensory signals given this dynamic uncertainty. Human psychophysical studies have shown that observers combine cues by weighting them in proportion to their reliability, consistent with statistically optimal integration schemes derived from Bayesian probability theory. Remarkably, because cue reliability is varied randomly across trials, the perceptual weight assigned to each cue must change from trial to trial. Dynamic cue reweighting has not been examined for combinations of visual and vestibular cues, nor has the Bayesian cue integration approach been applied to laboratory animals, an important step toward understanding the neural basis of cue integration. To address these issues, we tested human and monkey subjects in a heading discrimination task involving visual (optic flow) and vestibular (translational motion) cues. The cues were placed in conflict on a subset of trials, and their relative reliability was varied to assess the weights that subjects gave to each cue in their heading judgments. We found that monkeys can rapidly reweight visual and vestibular cues according to their reliability, the first such demonstration in a nonhuman species. However, some monkeys and humans tended to over-weight vestibular cues, inconsistent with simple predictions of a Bayesian model. Nonetheless, our findings establish a robust model system for studying the neural mechanisms of dynamic cue reweighting in multisensory perception.
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Project description:Perception is an inferential process, which becomes immediately evident when sensory information is conflicting or ambiguous and thus allows for more than one perceptual interpretation. Thinking the idea of perception as inference through to the end results in a blurring of boundaries between perception and action selection, as perceptual inference implies the construction of a percept as an active process. Here we therefore wondered whether perception shares a key characteristic of action selection, namely that it is shaped by reinforcement learning. In two behavioral experiments, we used binocular rivalry to examine whether perceptual inference can be influenced by the association of perceptual outcomes with reward or punishment, respectively, in analogy to instrumental conditioning. Binocular rivalry was evoked by two orthogonal grating stimuli presented to the two eyes, resulting in perceptual alternations between the two gratings. Perception was tracked indirectly and objectively through a target detection task, which allowed us to preclude potential reporting biases. Monetary reward or punishments were given repeatedly during perception of only one of the two rivaling stimuli. We found an increase in dominance durations for the percept associated with reward, relative to the non-rewarded percept. In contrast, punishment led to an increase of the non-punished compared to a relative decrease of the punished percept. Our results show that perception shares key characteristics with action selection, in that it is influenced by reward and punishment in opposite directions, thus narrowing the gap between the conceptually separated domains of perception and action selection. We conclude that perceptual inference is an adaptive process that is shaped by its consequences.
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