Article

Neural Correlates of Prior Expectations of Motion in the Lateral Intraparietal and Middle Temporal Areas

Department of Anatomy and Neurobiology, Washington University School of Medicine, Saint Louis, Missouri 63110, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.75). 07/2012; 32(29):10063-74. DOI: 10.1523/JNEUROSCI.5948-11.2012
Source: PubMed

ABSTRACT Successful decision making involves combining observations of the external world with prior knowledge. Recent studies suggest that neural activity in macaque lateral intraparietal area (LIP) provides a useful window into this process. This study examines how rapidly changing prior knowledge about an upcoming sensory stimulus influences the computations that convert sensory signals into plans for action. Two monkeys performed a cued direction discrimination task, in which an arrow cue presented at the start of each trial communicated the prior probability of the direction of stimulus motion. We hypothesized that the cue would either shift the initial level of LIP activity before sensory evidence arrived, or it would scale sensory responses according to the prior probability of each stimulus, manifesting as a change in slope of LIP firing rates. Neural recordings demonstrated a clear shift in the activity level of LIP neurons following the arrow cue, which persisted into the presentation of the motion stimulus. No significant change in slope of responses was observed, suggesting that sensory gain was not strongly modulated. To confirm the latter observation, middle temporal area (MT) neurons were recorded during a version of the cued direction discrimination task, and we found no change in MT responses resulting from the presentation of the directional cue. These results suggest that information about an immediately upcoming stimulus does not scale the sensory response, but rather changes the amount of evidence that must be accumulated to reach a decision in areas that are involved in planning action.

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Available from: Gregory C Deangelis, Jul 29, 2015
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    • "The combination of previous knowledge about the stimulus probability with incoming sensory evidence was extensively studied in two-alternative forced choice discrimination tasks (Forstmann et al., 2010; Hanks et al., 2011; Rao et al., 2012; Ratcliff and McKoon, 2008; Simen et al., 2009; Summerfield and Koechlin, 2008). These studies suggest that stationary priors are incorporated into the decision process as a shift in the amount of evidence needed to reach a decision. "
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    ABSTRACT: Under uncertainty, the brain uses previous knowledge to transform sensory inputs into the percepts on which decisions are based. When the uncertainty lies in the timing of sensory evidence, however, the mechanism underlying the use of previously acquired temporal information remains unknown. We study this issue in monkeys performing a detection task with variable stimulation times. We use the neural correlates of false alarms to infer the subject's response criterion and find that it modulates over the course of a trial. Analysis of premotor cortex activity shows that this modulation is represented by the dynamics of population responses. A trained recurrent network model reproduces the experimental findings and demonstrates a neural mechanism to benefit from temporal expectations in perceptual detection. Previous knowledge about the probability of stimulation over time can be intrinsically encoded in the neural population dynamics, allowing a flexible control of the response criterion over time. Copyright © 2015 Elsevier Inc. All rights reserved.
    Neuron 05/2015; 86(4). DOI:10.1016/j.neuron.2015.04.014 · 15.98 Impact Factor
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    • "We are suggesting that pursuit's priors for target speed and direction are created within the framework of pursuit's essential circuit. If this is true for all behaviors, and if priors are implemented downstream from the sensory representation (Rao et al., 2012), then each behavioral endpoint might implement Bayesian behavior through its own neural mechanism. The broad neural mechanism might be similar for different actions and different perceptions, but perception and action more generally could employ different neural mechanisms for prior formation. "
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    ABSTRACT: Sensory-motor behavior results from a complex interaction of noisy sensory data with priors based on recent experience. By varying the stimulus form and contrast for the initiation of smooth pursuit eye movements in monkeys, we show that visual motion inputs compete with two independent priors: one prior biases eye speed toward zero; the other prior attracts eye direction according to the past several days' history of target directions. The priors bias the speed and direction of the initiation of pursuit for the weak sensory data provided by the motion of a low-contrast sine wave grating. However, the priors have relatively little effect on pursuit speed and direction when the visual stimulus arises from the coherent motion of a high-contrast patch of dots. For any given stimulus form, the mean and variance of eye speed covary in the initiation of pursuit, as expected for signal-dependent noise. This relationship suggests that pursuit implements a trade-off between movement accuracy and variation, reducing both when the sensory signals are noisy. The tradeoff is implemented as a competition of sensory data and priors that follows the rules of Bayesian estimation. Computer simulations show that the priors can be understood as direction-specific control of the strength of visual-motor transmission, and can be implemented in a neural-network model that makes testable predictions about the population response in the smooth eye movement region of the frontal eye fields.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 12/2012; 32(49):17632-17645. DOI:10.1523/JNEUROSCI.1163-12.2012 · 6.75 Impact Factor
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    • "These observations lead the investigators to posit a novel modification to the drift diffusion model, where elapsed time is used to determine how much weight to apply to sensory evidence relative to prior probabilities. In contrast to those findings, another study manipulated prior probabilities (Rao et al., 2012) but found a largely additive effect on LIP responses instead. Such a modulation can of course be interpreted in terms of an additive offset of the accumulation of evidence, although it differs from the dynamic bias signal observed by Hanks and colleagues. "
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    ABSTRACT: A recent line of work has found remarkable success in relating perceptual decision-making and the spiking activity in the macaque lateral intraparietal area (LIP). In this review, we focus on questions about the neural computations in LIP that are not answered by demonstrations of neural correlates of psychological processes. We highlight three areas of limitations in our current understanding of the precise neural computations that might underlie neural correlates of decisions: (1) empirical questions not yet answered by existing data; (2) implementation issues related to how neural circuits could actually implement the mechanisms suggested by both extracellular neurophysiology and psychophysics; and (3) ecological constraints related to the use of well-controlled laboratory tasks and whether they provide an accurate window on sensorimotor computation. These issues motivate the adoption of a more general "encoding-decoding framework" that will be fruitful for more detailed contemplation of how neural computations in LIP relate to the formation of perceptual decisions.
    Frontiers in Integrative Neuroscience 10/2012; 6:86. DOI:10.3389/fnint.2012.00086
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