Instantaneous Midbrain Control of Saccade Velocity

Smalianchuk, Ivan; Jagadisan, Uday K.; Gandhi, Neeraj J.

doi:10.1523/jneurosci.0962-18.2018

Cited by 51 publications

(85 citation statements)

References 64 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The nucleus accumbens and ventral pallidum modulate their activity by reward expectation (Mohebi et al, 2019;Tachibana & Hikosaka, 2012), while the caudate nucleus is active when rewards are contingent on behaviour (Tricomi, Delgado, & Fiez, 2004). Both the caudate and accumbens/pallidum project to the output nuclei of the basal ganglia, allowing saccade initiation via the superior colliculus, which controls not only the direction of saccades, but also their instantaneous velocity during the movement (Smalianchuk, Jagadisan, & Gandhi, 2018). We propose contingent motivation and reward expectation both lead to motivational signals affecting the superior colliculus' activity controlling the velocity and acceleration of saccades, and these are differentially affected by dopamine ( Fig.6), although we remain agnostic as to the mechanism for this difference.…”

Section: Discussionmentioning

confidence: 99%

Dopamine promotes instrumental motivation, but reduces reward-related vigour

Grogan

Sandhu

et al. 2020

Preprint

View full text Add to dashboard Cite

We can be motivated when reward depends on performance, or merely by the prospect of a guaranteed reward. Performance-dependent (contingent) reward is instrumental, relying on an internal action-outcome model, whereas motivation by guaranteed reward may serve to minimise opportunity cost in reward-rich environments. Competing theories propose that each type of motivation should be dependent on dopaminergic activity. We contrasted these two types of motivation with a rewarded saccade task, in patients with Parkinson's disease (PD). When PD patients were ON dopamine, they had greater response vigour (peak saccadic velocity) for contingent rewards, whereas when PD patients were OFF medication, they had greater vigour for guaranteed rewards. These results support the view that reward expectation and contingency drive distinct motivational processes, and can be dissociated by manipulating dopaminergic activity. We posit that dopamine is necessary for goal-directed motivation, but dampens reward-driven vigour, challenging the theory that tonic dopamine encodes reward expectation.

show abstract

Section: Discussionmentioning

confidence: 99%

Dopamine promotes instrumental motivation, but reduces reward-related vigour

Grogan

Sandhu

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Because saccade vigor is dependent on activity of neurons in the superior colliculus [13], and these neurons are influenced by luminance and other low-level properties of the visual stimulus [14], the differences in vigor may have arisen not from presence of an RPE event, but rather because of other variables associated with differences in properties of the secondary image. Therefore, we included control trials in which the saccade of interest was made to the same image as in RPE trials, but without the benefit of an RPE event.…”

Section: Discussionmentioning

confidence: 99%

Reward prediction error modulates saccade vigor

Sedaghat-Nejad¹,

Herzfeld²,

Shadmehr³

2019

Preprint

View full text Add to dashboard Cite

Movements toward rewarding stimuli exhibit greater vigor, i.e., increased velocity and reduced reactiontimes. This invigoration may be due to release of dopamine before movement onset. Dopamine release is strongly modulated by reward prediction error (RPE). Here, we generated an RPE event in the milliseconds before movement onset and tested whether there was a causal relationship between RPE and vigor. Human subjects made saccades toward an image. During the execution of their primary saccade, we probabilistically changed the position and content of the image. This led to a secondary saccade following completion of the primary saccade. We focused on properties of this secondary saccade. On some trials, the content of the secondary image was more valuable than the first image, resulting in a +RPE event that preceded the secondary saccade. On other trials, this content was less valuable, resulting in a -RPE event. We found that reaction-time and velocity of the secondary saccade were affected in an orderly fashion by the magnitude and direction of the preceding RPE event: the most vigorous saccades followed the largest +RPE, whereas the least vigorous saccades followed the largest -RPE. Presence of the secondary saccade indicated that the primary saccade had experienced a movement error, inducing trial-to-trial adaptation: the subsequent primary saccade was changed in the direction of the movement error in the previous trial. However, motor learning from error was not affected by the RPE event. Therefore, reward prediction error, and not reward per se, modulated vigor of saccades. Author summaryDoes dopamine release before onset of a movement modulate vigor of the ensuing movement? To test this hypothesis, we relied on the fact that RPE is a strong modulator of dopamine. Our innovation was a task in which an RPE event occurred precisely before onset of a movement. We probabilistically produced a combination of large or small, negative or positive RPE events before onset of a saccade, and observed that the vigor of the saccade that followed carried a robust signature of the preceding RPE event: high vigor saccades followed +RPE events, while low vigor saccades followed -RPE events. This suggests that control of vigor is partly through release of dopamine in the moments before onset of the movement.

show abstract

“…Because saccade reaction time and velocity depend on activity of neurons in the superior colliculus (Smalianchuk et al, 2018) and these neurons are influenced by luminance and other lowlevel properties of the visual stimulus (Marino et al, 2015), the differences in vigor may have arisen not from presence of an RPE event, but rather because of other variables associated with differences in properties of the secondary image. Therefore, we included control trials in which the saccade of interest was made to the same image as in RPE trials, but without the benefit of an RPE event.…”

Section: Discussionmentioning

confidence: 99%

Reward Prediction Error Modulates Saccade Vigor

2019

View full text Add to dashboard Cite

Movement vigor, defined as the reciprocal of the latency from availability of reward to its acquisition, changes with reward magnitude: movements exhibit shorter reaction time and increased velocity when they are directed toward more rewarding stimuli. This invigoration may be due to release of dopamine before movement onset, which has been shown to be modulated by events that signal reward prediction error (RPE). Here, we generated an RPE event in the milliseconds before movement onset and tested whether there was a relationship between RPE and vigor. Human subjects (both sexes) made saccades toward an image. During execution of the primary saccade, we probabilistically changed the position and content of that image, encouraging a secondary saccade. On some trials, the content of the secondary image was more valuable than the first image, resulting in a positive RPE (ϩRPE) event that preceded the secondary saccade. On other trials, this content was less valuable (ϪRPE event). We found that reaction time of the secondary saccade was affected in an orderly fashion by the magnitude and direction of the preceding RPE event: the most vigorous saccades followed the largest ϩRPE, whereas the least vigorous saccades followed the largest ϪRPE. Presence of the secondary saccade indicated that the primary saccade had experienced a movement error, inducing trial-to-trial adaptation. However, this learning from movement error was not modulated by the RPE event. The data suggest that RPE events, which are thought to transiently alter the release of dopamine, modulate the vigor of the ensuing movement.

show abstract

Instantaneous Midbrain Control of Saccade Velocity

Cited by 51 publications

References 64 publications

Dopamine promotes instrumental motivation, but reduces reward-related vigour

Dopamine promotes instrumental motivation, but reduces reward-related vigour

Reward prediction error modulates saccade vigor

Reward Prediction Error Modulates Saccade Vigor

Contact Info

Product

Resources

About