skip to main content


Title: Separable Influences of Reward on Visual Processing and Choice
Primate vision is characterized by constant, sequential processing and selection of visual targets to fixate. Although expected reward is known to influence both processing and selection of visual targets, similarities and differences between these effects remain unclear mainly because they have been measured in separate tasks. Using a novel paradigm, we simultaneously measured the effects of reward outcomes and expected reward on target selection and sensitivity to visual motion in monkeys. Monkeys freely chose between two visual targets and received a juice reward with varying probability for eye movements made to either of them. Targets were stationary apertures of drifting gratings, causing the end points of eye movements to these targets to be systematically biased in the direction of motion. We used this motion-induced bias as a measure of sensitivity to visual motion on each trial. We then performed different analyses to explore effects of objective and subjective reward values on choice and sensitivity to visual motion to find similarities and differences between reward effects on these two processes. Specifically, we used different reinforcement learning models to fit choice behavior and estimate subjective reward values based on the integration of reward outcomes over multiple trials. Moreover, to compare the effects of subjective reward value on choice and sensitivity to motion directly, we considered correlations between each of these variables and integrated reward outcomes on a wide range of timescales. We found that, in addition to choice, sensitivity to visual motion was also influenced by subjective reward value, although the motion was irrelevant for receiving reward. Unlike choice, however, sensitivity to visual motion was not affected by objective measures of reward value. Moreover, choice was determined by the difference in subjective reward values of the two options, whereas sensitivity to motion was influenced by the sum of values. Finally, models that best predicted visual processing and choice used sets of estimated reward values based on different types of reward integration and timescales. Together, our results demonstrate separable influences of reward on visual processing and choice, and point to the presence of multiple brain circuits for the integration of reward outcomes.  more » « less
Award ID(s):
1632738
NSF-PAR ID:
10273512
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Journal of Cognitive Neuroscience
Volume:
33
Issue:
2
ISSN:
0898-929X
Page Range / eLocation ID:
248 to 262
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Perceptual decision-making has been shown to be influenced by reward expected from alternative options or actions, but the underlying neural mechanisms are currently unknown. More specifically, it is debated whether reward effects are mediated through changes in sensory processing, later stages of decision-making, or both. To address this question, we conducted two experiments in which human participants made saccades to what they perceived to be either the first or second of two visually identical but asynchronously presented targets while we manipulated expected reward from correct and incorrect responses on each trial. By comparing reward-induced bias in target selection (i.e., reward bias) during the two experiments, we determined whether reward caused changes in sensory or decision-making processes. We found similar reward biases in the two experiments indicating that reward information mainly influenced later stages of decision-making. Moreover, the observed reward biases were independent of the individual's sensitivity to sensory signals. This suggests that reward effects were determined heuristically via modulation of decision-making processes instead of sensory processing. To further explain our findings and uncover plausible neural mechanisms, we simulated our experiments with a cortical network model and tested alternative mechanisms for how reward could exert its influence. We found that our experimental observations are more compatible with reward-dependent input to the output layer of the decision circuit. Together, our results suggest that, during a temporal judgment task, reward exerts its influence via changing later stages of decision-making (i.e., response bias) rather than early sensory processing (i.e., perceptual bias). 
    more » « less
  2. Uncertainty permeates decisions from the trivial to the profound. Integrating brain and behavioral evidence, we discuss how probabilistic (varied outcomes) and temporal (delayed outcomes) uncertainty differ across age and individuals; how critical tests adjudicate between theories of uncertainty (prospect theory and fuzzy-trace theory); and how these mechanisms might be represented in the brain. The same categorical gist representations of gains and losses account for choices and eye-tracking data in both value-allocation (add money to gambles) and risky-choice tasks, disconfrming prospect theory and confrming predictions of fuzzy-trace theory. The analysis is extended to delay discounting and disambiguated choices, explaining hidden zero effects that similarly turn on categorical distinctions between some gain and no gain, certain gain and uncertain gain, gain and loss, and now and later. Bold activation implicates dorsolateral prefrontal and posterior parietal cortices in gist strategies that are not just one tool in a grab-bag of cognitive options but rather are general strategies that systematically predict behaviors across many different tasks involving probabilistic and temporal uncertainty. High valuation (e.g., ventral striatum; ventromedial prefrontal cortex) and low executive control (e.g., lateral prefrontal cortex) contribute to risky and impatient choices, especially in youth. However, valuation in ventral striatum supports reward-maximizing and gist strategies in adulthood. Indeed, processing becomes less “rational” in the sense of maximizing gains and more noncompensatory (eye movements indicate fewer tradeoffs) as development progresses from adolescence to adulthood, as predicted. Implications for theoretically predicted “public-health paradoxes” are discussed, including gist versus verbatim thinking in drug experimentation and addiction. 
    more » « less
  3. Objective: To determine if a vestibular prosthesis could improve function in subjects with severe vestibular damage and could be used it as a scientific tool to investigate central vestibular processing. Background: Damage to the vestibular labyrinth is common and usually permanent. We therefore developed and tested a vestibular implant (VI) that is designed to mimic the information normally provided by the vestibular labyrinth to determine if we can reduce vestibular-mediated deficits and study temporal integration of sensory cues in the brain. Design/Methods: Monkeys had electrodes implanted in the semicircular canals of one ear and then severe bilateral vestibular damage was induced with aminoglycosides. Eye movements, perception, and balance were tested before and after vestibular damage and with the VI activated, which supplied head motion information to the brain via electrical stimulation delivered by the implanted electrodes. Humans also had electrode implantation (done in conjunction with a cochlear implant, CI) and they were tested on a temporal binding psychophysical task Results: Stimulation provided by VI in vestibulopathic monkeys improved their balance, perception of spatial orientation, and eye movement responses. Timing experiments in humans using CI and VI stimuli showed that unlike past experiments that used motion to generate the vestibular signal, CI and VI signals were received by the cerebral cortex with the same latency and were perceived as simultaneous, but this timing perception was highly sensitive to adaption. Conclusions: VI improves oculomotor, postural, and perceptual behavior in vestibulopathic monkeys and could prove to be an effective way to improve these functions in patients with permanent labyrinthine damage. Timing experiments show that when novel stimuli are used, the brain synthesizes them in accordance with their arrival at the cortex, but that experience can rapidly recalibrate this timing relationship, which may be why normal stimuli that are experienced habitually lack this characteristic. 
    more » « less
  4. Abstract

    Deliberation is thought to involve the internal simulation of the outcomes of candidate actions, the valuation of those outcomes, and the selection of the actions with the highest expected value. While it is known that deliberation involves prefrontal cortical areas, specifically the dorsomedial prefrontal cortex (dmPFC), as well as the hippocampus (HPC) and other brain regions, how these areas process prospective information and select actions is not well understood. We recorded simultaneously from ensembles in dmPFC and CA1 of dorsal HPC in rats during performance of a spatial contingency switching task, and examined the relationships between spatial and reward encoding in these two areas during deliberation at the choice point. We found that CA1 and dmPFC represented either goal locations or the current position simultaneously, but that when goal locations were encoded, HPC and dmPFC did not always represent the same goal location. Ensemble activity in dmPFC predicted when HPC would represent goal locations, but on a broad timescale on the order of seconds. Also, reward encoding in dmPFC increased during hippocampal theta cycles where CA1 ensembles represented the goal location. These results suggest that dmPFC and HPC share prospective information during deliberation, that dmPFC may influence whether HPC represents prospective information, and that information recalled about goal locations by HPC may be integrated into dmPFC reward representations on fast timescales.

     
    more » « less
  5. Abstract

    In perceptual decisions, subjects infer hidden states of the environment based on noisy sensory information. Here we show that both choice and its associated confidence are explained by a Bayesian framework based on partially observable Markov decision processes (POMDPs). We test our model on monkeys performing a direction-discrimination task with post-decision wagering, demonstrating that the model explains objective accuracy and predicts subjective confidence. Further, we show that the model replicates well-known discrepancies of confidence and accuracy, including the hard-easy effect, opposing effects of stimulus variability on confidence and accuracy, dependence of confidence ratings on simultaneous or sequential reports of choice and confidence, apparent difference between choice and confidence sensitivity, and seemingly disproportionate influence of choice-congruent evidence on confidence. These effects may not be signatures of sub-optimal inference or discrepant computational processes for choice and confidence. Rather, they arise in Bayesian inference with incomplete knowledge of the environment.

     
    more » « less