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: 6.34). 07/2012; 32(29):10063-74. DOI: 10.1523/JNEUROSCI.5948-11.2012
Source: PubMed


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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    • "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.
    Full-text · Article · May 2015 · Neuron
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    • "An interpretation of these results is that LIP plays a more central role in nonspatial cognitive processing than is often assumed, especially during complex behavioral tasks that require abstraction, working memory, or flexible sensory-motor mappings. This is consistent with a number of studies that found encoding of nonspatial and/or cognitive factors in parietal cortex (Sereno and Maunsell, 1998; Toth and Assad, 2002; Nieder et al., 2006; Oristaglio et al., 2006; Gottlieb and Snyder, 2010; Rao et al., 2012), and recent work suggests that LIP could be a source of these cognitive signals to other brain areas. For example, we recently demonstrated that LIP shows a strongerand shorter-latency encoding of motion categories than the lateral PFC (Swaminathan and Freedman, 2012) and that explicit category signals are not observed in MT (Freedman and Assad, 2006), a key motion-processing area (Born and Bradley, 2005) that provides input to LIP (Lewis and Van Essen, 2000). "
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    ABSTRACT: The posterior parietal cortex plays a central role in spatial functions, such as spatial attention and saccadic eye movements. However, recent work has increasingly focused on the role of parietal cortex in encoding nonspatial cognitive factors such as visual categories, learned stimulus associations, and task rules. The relationship between spatial encoding and nonspatial cognitive signals in parietal cortex, and whether cognitive signals are robustly encoded in the presence of strong spatial neuronal responses, is unknown. We directly compared nonspatial cognitive and spatial encoding in the lateral intraparietal (LIP) area by training monkeys to perform a visual categorization task during which they made saccades toward or away from LIP response fields (RFs). Here we show that strong saccade-related responses minimally influence robustly encoded category signals in LIP. This suggests that cognitive and spatial signals are encoded independently in LIP and underscores the role of parietal cortex in nonspatial cognitive functions. VIDEO ABSTRACT:
    Preview · Article · Mar 2013 · Neuron
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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.
    Preview · Article · Dec 2012 · The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
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