Frontal eye field and caudate neurons make different contributions to reward-biased perceptual decisions

Many decisions require trade-offs between sensory evidence and internal preferences. Potential neural substrates include the frontal eye field (FEF) and caudate nucleus, but their distinct roles are not understood. Previously we showed that monkeys’ decisions on a direction-discrimination task with asymmetric rewards reflected a biased accumulate-to-bound decision process (Fan et al., 2018) that was affected by caudate microstimulation (Doi et al., 2020). Here we compared single-neuron activity in FEF and caudate to each other and to accumulate-to-bound model predictions derived from behavior. Task-dependent neural modulations were similar in both regions. However, choice-selective neurons in FEF, but not caudate, encoded behaviorally derived biases in the accumulation process. Baseline activity in both regions was sensitive to reward context, but this sensitivity was not reliably associated with behavioral biases. These results imply distinct contributions of FEF and caudate neurons to reward-biased decision-making and put experimental constraints on the neural implementation of accumulation-to-bound-like computations.

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Contrasting the roles of the supplementary and frontal eye fields in ocular decision making

Journal of Neurophysiology ◽

10.1152/jn.00543.2013 ◽

2014 ◽

Vol 111 (12) ◽

pp. 2644-2655 ◽

Cited By ~ 13

Author(s):

Shun-nan Yang ◽

Stephen Heinen

Keyword(s):

Decision Making ◽

Single Neuron ◽

Delay Period ◽

Neuron Activity ◽

Frontal Eye Field ◽

Unit Recording ◽

Task Rule ◽

Supplementary Eye Field ◽

Eye Field ◽

Single Neuron Activity

Single-unit recording in monkeys and functional imaging of the human frontal lobe indicate that the supplementary eye field (SEF) and the frontal eye field (FEF) are involved in ocular decision making. To test whether these structures have distinct roles in decision making, single-neuron activity was recorded from each structure while monkeys executed an ocular go/nogo task. The task rule is to pursue a moving target if it intersects a visible square or “go zone.” We found that most SEF neurons showed differential go/nogo activity during the delay period, before the target intersected the go zone (delay period), whereas most FEF neurons did so after target intersection, during the period in which the movement was executed (movement period). Choice probability (CP) for SEF neurons was high in the delay period but decreased in the movement period, whereas for FEF neurons it was low in the delay period and increased in the movement period. Directional selectivity of SEF neurons was low throughout the trial, whereas that of FEF neurons was highest in the delay period, decreasing later in the trial. Increasing task difficulty led to later discrimination between go and nogo in both structures and lower CP in the SEF, but it did not affect CP in the FEF. The results suggest that the SEF interprets the task rule early but is less involved in executing the motor decision than is the FEF and that these two areas collaborate dynamically to execute ocular decisions.

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Perceptual modulation of parietal activity during urgent saccadic choices

10.1101/2019.12.12.874313 ◽

2019 ◽

Author(s):

Joshua A. Seideman ◽

Emilio Salinas ◽

Terrence R. Stanford

Keyword(s):

Time Course ◽

Single Neuron ◽

Motor Planning ◽

Neuron Activity ◽

Lateral Intraparietal Cortex ◽

Perceptual Evaluation ◽

Visuomotor Transformations ◽

Sensory Evidence ◽

Definition Of ◽

Single Neuron Activity

The lateral intraparietal cortex (LIP) contributes to visuomotor transformations for determining where to look next. However, its spatial selectivity can signify attentional priority, motor planning, perceptual discrimination, or other mechanisms. Resolving how this LIP signal influences a perceptually guided choice requires knowing exactly when such signal arises and when the perceptual evaluation informs behavior. To achieve this, we recorded single-neuron activity while monkeys performed an urgent choice task for which the perceptual evaluation’s progress can be tracked millisecond by millisecond. The evoked presaccadic responses were strong, exhibited modest motor preference, and were only weakly modulated by sensory evidence. This modulation was remarkable, though, in that its time course preceded and paralleled that of behavioral performance (choice accuracy), and it closely resembled the statistical definition of confidence. The results indicate that, as the choice process unfolds, LIP dynamically combines attentional, motor, and perceptual signals, the former being much stronger than the latter.

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Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets

eLife ◽

10.7554/elife.33456 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 12

Author(s):

Christopher K Hauser ◽

Dantong Zhu ◽

Terrence R Stanford ◽

Emilio Salinas

Keyword(s):

Reaction Time ◽

Single Neuron ◽

Frontal Eye Field ◽

Initial State ◽

Baseline Activity ◽

Selection Dynamics ◽

Computational Work ◽

Eye Field ◽

Threshold Process ◽

Oculomotor Activity

In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.

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