A neural correlate of response bias in monkey caudate nucleus

Abstract

Primates are equipped with neural circuits in the prefrontal cortex, the parietal cortex and the basal ganglia that predict the availability of reward during the performance of behavioural tasks. It is not known, however, how reward value is incorporated in the control of action. Here we identify neurons in the monkey caudate nucleus that create a spatially selective response bias depending on the expected gain. In behavioural tasks, the monkey had to make a visually guided eye movement in every trial, but was rewarded for a correct response in only half of the trials. Reward availability was predictable on the basis of the spatial position of the visual target. We found that caudate neurons change their discharge rate systematically, even before the appearance of the visual target, and usually fire more when the contralateral position is associated with reward. Strong anticipatory activity of neurons with a contralateral preference is associated with decreased latency for eye movements in the contralateral direction. We conclude that this neuronal mechanism creates an advance bias that favours a spatial response when it is associated with a high reward value.

Linking reward expectation to behavior in the basal ganglia

“…Several recent studies have characterized the influence of reward expectation on neural circuits involved in sensory-motor transformations [14,16 -20]. The study by Lauwereyns and colleagues [4] adds to that short list and provides novel insights into how the brain might use signals related to a spatially selective anticipation of reward to bias a simple oculomotor behavior. It will be interesting to see whether the same principles can be extended to include other factors and more complex behaviors.…”

“…For example, despite a growing body of work identifying neural circuits that represent information related to reward in the context of sensory -motor tasks [3], how these kinds of signals might influence behavior is a mystery. A recent study by Lauwereyns and colleagues has begun to shed light on this difficult issue [4]. The results describe neural signals in a region of the basal ganglia called the caudate nucleus that appear to relate anticipation of an uncertain reward with the preparation for a goal-directed eye movement.…”

“…Hippocampal theta rhythm is a low frequency (5-10 Hz) oscillation of extracellular current that results from the collective activity of groups of neurons ( [1]; reviewed in Refs [2][3][4]). This network oscillation occurs during a wide variety of spatial and non-spatial behaviors and can be thought of as a type of timing signal, upon which the action…”

Dopaminergic and non-dopaminergic value systems in conditioning and outcome-specific revaluation

“…(Nakamura et al, 1992;Braesicke et al, 2005). Motivational influences on saccadic reaction time are reproduced using incentive value signals broadcast by orbitofrontal cortex (Lauwereyns et al, 2002;Roesch and Olson, 2003). 3a: Simulated blood pressure output (right) compared with recorded blood pressure (left) during CS Task performance [Reprinted with permission from Nakamura et al (1992)].…”

“…Saccadic response time (SRT) is correlated with the time it takes a visually-selective FEF cell to respond to a target in its receptive field during visual discrimination (Sato et al, 2001). Numerous studies have demonstrated that target salience is one of the attributes that can speed the discrimination of targets from distractors (Lauwereyns et al, 2002;Roesch and Olson, 2004). Incentive motivation also impacts SRT, but the timing of instrumental saccades involves dorsal striatal mechanisms (Corbit et al, 2001;Brown et al, 2004).…”