Reward Prediction Error Modulates Saccade Vigor

Sedaghat-Nejad, Ehsan; Herzfeld, David J.; Shadmehr, Reza

doi:10.1523/jneurosci.0432-19.2019

Cited by 45 publications

(26 citation statements)

References 33 publications

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“…Yet, we still observed a pronounced change in accuracy post-muscimol even for the 36% coherence condition, a finding that is better explained by a change in aspects of decision-making, rather than a motor preference under uncertainty. Also, if we assumed the monkeys opted for easier awayIF saccades, we reasoned that toIF saccades in the decision task should be harder to make and therefore slower, than saccades in the selection task, given that slower saccades indicate reduced vigor 12 . Interestingly, in some cases, the velocity of toIF saccades in the decision task was higher than those in the selection task after muscimol, despite matched metrics (cf., cyan symbols in post in Fig.…”

Section: Decision But Not Selection Accuracy Is Altered After Sc Inacmentioning

confidence: 99%

Embodied Cognition and Decision-Making in the Primate Superior Colliculus

Jun¹,

Bautista²,

Nunez³

et al. 2020

Preprint

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A popular model of decision-making suggests that in primates, including humans, decisions evolve within forebrain structures responsible for preparing voluntary actions; a concert referred to as embodied cognition. Embodied cognition posits that in decision tasks, neuronal activity generally associated with preparing an action, actually reflects the accumulation of evidence for a particular decision. Testing the embodied cognition model causally is challenging because dissociating the evolution of a decision from preparing a motor act is difficult, if the same neuronal activity instantiates both processes. Ideally, one would show that manipulation of neuronal activity thought to be involved in movement preparation actually alters decisions, and not movement preparation. Here, trained monkeys performed a two-choice perceptual decision-making task in which they judged the orientation of a dynamic Glass pattern before and after unilateral, reversible inactivation of a brainstem area involved in preparing eye movements, the superior colliculus (SC). Surprisingly, we found that unilateral SC inactivation produced significant decision biases and changes in reaction times consistent with a role for the SC in evidence accumulation. Fitting signal detection theory and sequential sampling models (drift-diffusion and urgency-gating) to the data revealed that SC inactivation produced a decrease in the relative evidence for contralateral decisions. Control experiments showed that SC inactivation did not result in eye movement biases ruling out interpretations based on motor preparation or spatial attentional impairment. The results provide causal evidence for an embodied cognition model of perceptual decision-making and provide compelling evidence that the SC of primates plays a causal role in modulating evidence accumulation for perceptual decisions, a process that is usually attributed to the cerebral cortex.

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Section: Decision But Not Selection Accuracy Is Altered After Sc Inacmentioning

confidence: 99%

Embodied Cognition and Decision-Making in the Primate Superior Colliculus

Jun¹,

Bautista²,

Nunez³

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Notably, in children with ASD, we found that damage to the cerebellum is prevalent in lobule VI and parts of lobule VIII (Marko et al 2015), regions that in the macaque are critical for control of saccadic eye movements (Barash et al 1999;Takagi et al 1998). Control of saccades in healthy subjects shows exquisite sensitivity to decision-related variables such as reward prediction error (Sedaghat-Nejad et al 2019) and history of effort expenditure (Yoon et al 2018). Thus marmosets may present a particularly good opportunity to investigate the role of the cerebellum in eye movements, social communication, and neurological diseases such as ASD.…”

Section: Introductionmentioning

confidence: 97%

Behavioral training of marmosets and electrophysiological recording from the cerebellum

Sedaghat-Nejad

Herzfeld

Hage

et al. 2019

Journal of Neurophysiology

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The common marmoset ( Callithrix jacchus) is a promising new model for study of neurophysiological basis of behavior in primates. Like other primates, it relies on saccadic eye movements to monitor and explore its environment. Previous reports have demonstrated some success in training marmosets to produce goal-directed actions in the laboratory. However, the number of trials per session has been relatively small, thus limiting the utility of marmosets as a model for behavioral and neurophysiological studies. In this article, we report the results of a series of new behavioral training and neurophysiological protocols aimed at increasing the number of trials per session while recording from the cerebellum. To improve the training efficacy, we designed a precisely calibrated food regulation regime that motivates the subjects to perform saccade tasks, resulting in ~1,000 reward-driven trials on a daily basis. We then developed a multichannel recording system that uses imaging to target a desired region of the cerebellum, allowing for simultaneous isolation of multiple Purkinje cells in the vermis. In this report, we describe 1) the design and surgical implantation of a computer tomography (CT)-guided, subject-specific head post, 2) the design of a CT- and MRI-guided alignment tool for trajectory guidance of electrodes mounted on an absolute encoder microdrive, 3) development of a protocol for behavioral training of subjects, and 4) simultaneous recordings from pairs of Purkinje cells during a saccade task. NEW & NOTEWORTHY Marmosets present the opportunity to investigate genetically based neurological disease in primates, in particular, diseases that affect social behaviors, vocal communication, and eye movements. All of these behaviors depend on the integrity of the cerebellum. We present training methods that better motivate the subjects, allowing for improved performance, and we also present electrophysiological techniques that precisely target the subject’s cerebellum, allowing for simultaneous isolation of multiple Purkinje cells.

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“…Minimization of an overall performance cost has also been suggested by others to underlie oculomotor behavior (for eye saccades, Harris and Wolpert, 2006 ; Sadaghat-Nejad et al, 2019 ). As the human fovea has a high resolution within only 1° of visual angle, and considerable uncertainty in the retinal periphery, theoretical studies have indicated that the saccadic system aims to optimize speed-accuracy trade-off, to minimize saccade duration at the smallest mean-absolute localization errors ( Harris and Wolpert, 2006 ).…”

Section: Discussionmentioning

confidence: 83%

Adaptive Response Behavior in the Pursuit of Unpredictably Moving Sounds

Calvo¹,

Wanrooij²,

Opstal³

2021

eNeuro

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Although moving sound-sources abound in natural auditory scenes, it is not clear how the human brain processes auditory motion. Previous studies have indicated that, although ocular localization responses to stationary sounds are quite accurate, ocular smooth pursuit of moving sounds is very poor. We here demonstrate that human subjects faithfully track a sound’s unpredictable movements in the horizontal plane with smooth-pursuit responses of the head. Our analysis revealed that the stimulus–response relation was well described by an under-damped passive, second-order low-pass filter in series with an idiosyncratic, fixed, pure delay. The model contained only two free parameters: the system’s damping coefficient, and its central (resonance) frequency. We found that the latter remained constant at ∼0.6 Hz throughout the experiment for all subjects. Interestingly, the damping coefficient systematically increased with trial number, suggesting the presence of an adaptive mechanism in the auditory pursuit system (APS). This mechanism functions even for unpredictable sound-motion trajectories endowed with fixed, but covert, frequency characteristics in open-loop tracking conditions. We conjecture that the APS optimizes a trade-off between response speed and effort. Taken together, our data support the existence of a pursuit system for auditory head-tracking, which would suggest the presence of a neural representation of a spatial auditory fovea (AF).

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Reward Prediction Error Modulates Saccade Vigor

Cited by 45 publications

References 33 publications

Embodied Cognition and Decision-Making in the Primate Superior Colliculus

Embodied Cognition and Decision-Making in the Primate Superior Colliculus

Behavioral training of marmosets and electrophysiological recording from the cerebellum

Adaptive Response Behavior in the Pursuit of Unpredictably Moving Sounds

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