Dataset Information

A causal role for V5/MT neurons coding motion-disparity conjunctions in resolving perceptual ambiguity.

ABSTRACT: Judgments about the perceptual appearance of visual objects require the combination of multiple parameters, like location, direction, color, speed, and depth. Our understanding of perceptual judgments has been greatly informed by studies of ambiguous figures, which take on different appearances depending upon the brain state of the observer. Here we probe the neural mechanisms hypothesized as responsible for judging the apparent direction of rotation of ambiguous structure from motion (SFM) stimuli. Resolving the rotation direction of SFM cylinders requires the conjoint decoding of direction of motion and binocular depth signals [1, 2]. Within cortical visual area V5/MT of two macaque monkeys, we applied electrical stimulation at sites with consistent multiunit tuning to combinations of binocular depth and direction of motion, while the monkey made perceptual decisions about the rotation of SFM stimuli. For both ambiguous and unambiguous SFM figures, rotation judgments shifted as if we had added a specific conjunction of disparity and motion signals to the stimulus elements. This is the first causal demonstration that the activity of neurons in V5/MT contributes directly to the perception of SFM stimuli and by implication to decoding the specific conjunction of disparity and motion, the two different visual cues whose combination drives the perceptual judgment.

SUBMITTER: Krug K

PROVIDER: S-EPMC3739008 | biostudies-literature | 2013 Aug

REPOSITORIES: biostudies-literature

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A causal role for V5/MT neurons coding motion-disparity conjunctions in resolving perceptual ambiguity.

Krug Kristine K Cicmil Nela N Parker Andrew J AJ Cumming Bruce G BG

Current biology : CB 20130718 15

Judgments about the perceptual appearance of visual objects require the combination of multiple parameters, like location, direction, color, speed, and depth. Our understanding of perceptual judgments has been greatly informed by studies of ambiguous figures, which take on different appearances depending upon the brain state of the observer. Here we probe the neural mechanisms hypothesized as responsible for judging the apparent direction of rotation of ambiguous structure from motion (SFM) stim ...[more]

PMID: 23871244

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Project description:Cortical neurons are frequently tuned to several stimulus dimensions, and many cortical areas contain intercalated maps of multiple variables. Relatively little is known about how information is "read out" of these multidimensional maps. For example, how does an organism extract information relevant to the task at hand from neurons that are also tuned to other, irrelevant stimulus dimensions? We addressed this question by employing microstimulation techniques to examine the contribution of disparity-tuned neurons in the middle temporal (MT) visual area to performance on a direction discrimination task. Most MT neurons are tuned to both binocular disparity and the direction of stimulus motion, and MT contains topographic maps of both parameters. We assessed the effect of microstimulation on direction judgments after first characterizing the disparity tuning of each stimulation site. Although the disparity of the stimulus was irrelevant to the required task, we found that microstimulation effects were strongly modulated by the disparity tuning of the stimulated neurons. For two of three monkeys, microstimulation of nondisparity-selective sites produced large biases in direction judgments, whereas stimulation of disparity-selective sites had little or no effect. The binocular disparity was optimized for each stimulation site, and our result could not be explained by variations in direction tuning, response strength, or any other tuning property that we examined. When microstimulation of a disparity-tuned site did affect direction judgments, the effects tended to be stronger at the preferred disparity of a stimulation site than at the nonpreferred disparity, indicating that monkeys can selectively monitor direction columns that are best tuned to an appropriate conjunction of parameters. We conclude that the contribution of neurons to behavior can depend strongly upon tuning to stimulus dimensions that appear to be irrelevant to the current task, and we suggest that these findings are best explained in terms of the strategy used by animals to perform the task.

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

A causal role for V5/MT neurons coding motion-disparity conjunctions in resolving perceptual ambiguity.

Publications

A causal role for V5/MT neurons coding motion-disparity conjunctions in resolving perceptual ambiguity.

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