The caudate nucleus contributes causally to decisions that balance reward and uncertain visual information.
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ABSTRACT:
SUBMITTER: Doi T
PROVIDER: S-EPMC7308093 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:While the role of cortical regions in cognitive control processes is well accepted, the contribution of subcortical structures (e.g., the striatum), especially to the control of response interference, remains controversial. Therefore, the present study aimed to investigate the cortical and particularly subcortical neural mechanisms of response interference control (including selective inhibition). Thirteen healthy young participants underwent event-related functional magnetic resonance imaging while performing a unimanual version of the Simon task. In this task, successful performance required the resolution of stimulus-response conflicts in incongruent trials by selectively inhibiting interfering response tendencies. The behavioral results show an asymmetrical Simon effect that was more pronounced in the contralateral hemifield. Contrasting incongruent trials with congruent trials (i.e., the overall Simon effect) significantly activated clusters in the right anterior cingulate cortex, the right posterior insula, and the caudate nucleus bilaterally. Furthermore, a region of interest analysis based on previous patient studies revealed that activation in the bilateral caudate nucleus significantly co-varied with a parameter of selective inhibition derived from distributional analyses of response times. Our results corroborate the notion that the cognitive control of response interference is supported by a fronto-striatal circuitry, with a functional contribution of the caudate nucleus to the selective inhibition of interfering response tendencies.
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Project description: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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Project description:Expected reward impacts behavior and neuronal activity in brain areas involved in sensorimotor processes. However, where and how reward signals affect sensorimotor signals is unclear. Here, we show evidence that reward-dependent modulation of behavior depends on normal dopamine transmission in the striatum. Monkeys performed a visually guided saccade task in which expected reward gain was different depending on the position of the target. Saccadic reaction times were reliably shorter on large-reward trials than on small-reward trials. When position-reward contingency was switched, the reaction time difference changed rapidly. Injecting dopamine D1 antagonist into the caudate significantly attenuated the reward-dependent saccadic reaction time changes. Conversely, injecting D2 antagonist into the same region enhanced the reward-dependent changes. These results suggest that reward-dependent changes in saccadic eye movements depend partly on dopaminergic modulation of neuronal activity in the caudate nucleus.
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Project description:When searching for an object, we use a target template in memory that contains task-relevant information to guide visual attention to potential targets and to determine the identity of attended objects. These processes in visual search have typically been assumed to rely on a common source of template information. However, our recent work (Yu et al., 2022) argued that attentional guidance and target-match decisions rely on different information during search, with guidance using a "fuzzier" version of the template compared with target decisions. However, that work was based on the special case of search for a target amongst linearly separable distractors (e.g., search for an orange target amongst yellower distractors). Real-world search targets, however, are infrequently linearly separable from distractors, and it remains unclear whether the differences between the precision of template information used for guidance compared with target decisions also applies under more typical conditions. In four experiments, we tested this question by varying distractor similarity during visual search and measuring the likelihood of attentional guidance to distractors and target misidentifications. We found that early attentional guidance is indeed less precise than that of subsequent match decisions under varying exposure durations and distractor set sizes. These results suggest that attentional guidance operates on a coarser code than decisions, perhaps because guidance is constrained by lower acuity in peripheral vision or the need to rapidly explore a wide region of space while decisions about selected objects are more precise to optimize decision accuracy.
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Project description:Saccadic eye movements are the result of neural decisions about where to move the eyes. These decisions are based on visual information accumulated before the saccade; however, during an approximately 100-ms interval immediately before the initiation of an eye movement, new visual information cannot influence the decision. Does the brain simply ignore information presented during this brief interval or is the information used for the subsequent saccade? Our study examines how and when the brain integrates visual information through time to drive saccades during visual search. We introduce a new technique, saccade-contingent reverse correlation, that measures the time course of visual information accrual driving the first and second saccades. Observers searched for a contrast-defined target among distractors. Independent contrast noise was added to the target and distractors every 25 ms. Only noise presented in the time interval in which the brain accumulates information will influence the saccadic decisions. Therefore, we can retrieve the time course of saccadic information accrual by averaging the time course of the noise, aligned to saccade initiation, across all trials with saccades to distractors. Results show that before the first saccade, visual information is being accumulated simultaneously for the first and second saccades. Furthermore, information presented immediately before the first saccade is not used in making the first saccadic decision but instead is stored and used by the neural processes driving the second saccade.
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Project description:ObjectiveThe object of this study was to define caudate nucleus locations responsive to intraoperative direct electrical stimulation for tinnitus loudness modulation and relate those locations to functional connectivity maps between caudate nucleus subdivisions and auditory cortex.MethodsSix awake study participants who underwent bilateral deep brain stimulation (DBS) electrode placement in the caudate nucleus as part of a phase I clinical trial were analyzed for tinnitus modulation in response to acute stimulation at 20 locations. Resting-state 3-T functional MRI (fMRI) was used to compare connectivity strength between centroids of tinnitus loudness-reducing or loudness-nonreducing caudate locations and the auditory cortex in the 6 DBS phase I trial participants and 14 other neuroimaging participants with a Tinnitus Functional Index > 50.ResultsAcute tinnitus loudness reduction was observed at 5 caudate locations, 4 positioned at the body and 1 at the head of the caudate nucleus in normalized Montreal Neurological Institute space. The remaining 15 electrical stimulation interrogations of the caudate head failed to reduce tinnitus loudness. Compared to the caudate head, the body subdivision had stronger functional connectivity to the auditory cortex on fMRI (p < 0.05).ConclusionsAcute tinnitus loudness reduction was more readily achieved by electrical stimulation of the caudate nucleus body. Compared to the caudate head, the caudate body has stronger functional connectivity to the auditory cortex. These first-in-human findings provide insight into the functional anatomy of caudate nucleus subdivisions and may inform future target selection in a basal ganglia-centric neuromodulation approach to treat medically refractory tinnitus.Clinical trial registration no.: NCT01988688 (clinicaltrials.gov).
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