Reward-related neuronal activity in the subthalamic nucleus of the monkey

Laboratoire de Neurobiologie de la Cognition, CNRS, 31 chemin Joseph Aiguier, 13402 Marseille cedex 20, France.
Neuroreport (Impact Factor: 1.52). 09/2005; 16(11):1241-4. DOI: 10.1097/00001756-200508010-00022
Source: PubMed


The subthalamic nucleus is a key structure for motor information processing in the basal ganglia. Little is known about its involvement in other aspects of behavior such as motivation. We investigated neuronal activity in the subthalamic nucleus while a monkey performed arm-reaching movements to obtain a liquid reward. Most neurons were modulated both during the movement and reward phases of the task. The changes in activity occurring after or just before the delivery of reward consisted of either increases or decreases in firing and were not directly related to mouth movements. These findings indicate that STN neurons are involved in the detection and expectation of reward, consistent with a role for these neurons in the processing of motivational information.

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    • "Differences in firing rate between conditions (e.g., match vs. non-match) were tested with ANOVA using a 100-ms sliding window, advancing in 20-ms increments (cf. Apicella et al., 1997; Darbaky et al., 2005; Chandrasekaran and Ghazanfar, 2009). Effects were only considered significant in cases where significant differences (p < 0.05) were obtained for two or more consecutive steps. "
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    ABSTRACT: Behaviorally-relevant sounds such as conspecific vocalizations are often available for only a brief amount of time; thus, goal-directed behavior frequently depends on auditory short-term memory (STM). Despite its ecological significance, the neural processes underlying auditory STM remain poorly understood. To investigate the role of the auditory cortex in STM, single-and multi-unit activity was recorded from the primary auditory cortex (A1) of two monkeys performing an auditory STM task using simple and complex sounds. Each trial consisted of a sample and test stimulus separated by a 5-s retention interval. A brief wait period followed the test stimulus, after which subjects pressed a button if the sounds were identical (match trials) or withheld button presses if they were different (non-match trials). A number of units exhibited significant changes in firing rate for portions of the retention interval, although these changes were rarely sustained. Instead, they were most frequently observed during the early and late portions of the retention interval, with inhibition being observed more frequently than excitation. At the population level, responses elicited on match trials were briefly suppressed early in the sound period relative to non-match trials. However, during the latter portion of the sound, firing rates increased significantly for match trials and remained elevated throughout the wait period. Related patterns of activity were observed in prior experiments from our lab in the dorsal temporal pole (dTP) and prefrontal cortex (PFC) of the same animals. The data suggest that early match suppression occurs in both A1 and the dTP, whereas later match enhancement occurs first in the PFC, followed by A1 and later in dTP. Because match enhancement occurs first in the PFC, we speculate that enhancement observed in A1 and dTP may reflect top–down feedback. Overall, our findings suggest that A1 forms part of the larger neural system recruited during auditory STM.
    Frontiers in Neuroscience 08/2014; 8(8). DOI:10.3389/fnins.2014.00250 · 3.66 Impact Factor
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    • "In particular, neurons sensitive to reward were scattered throughout the parts of the STN explored, without preferential location in the ventromedial part, which receives inputs from the orbitofrontal cortex and anterior cingulate cortex and is considered the « limbic » part of the STN in primates (Takada et al., 2001; Karachi et al., 2005; Haynes and Haber, 2013). This observation confirms what had been previously noted in our preliminary study (Darbaky et al., 2005). Also, neurons sensitive to movement did not appear to be clustered in the dorsolateral part of the STN, which is connected to motor and premotor cortical areas, and corresponds to the « motor »part of the STN. "
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    ABSTRACT: The expectation and detection of motivationally relevant events is a major determinant of goal-directed behavior and there is a strong interest in the contribution of basal ganglia in the integration of motivational processes into behavioral output. Recent research has focused on the role of the subthalamic nucleus (STN) in the motivational control of action, but it remains to be determined how information about reward is encoded in this nucleus. We recorded the activity of single neurons in the STN of two behaving monkeys to examine whether activity was influenced by the delivery of reward in an instrumental task, a Pavlovian stimulus-reward association, or outside of a task context. We confirmed preliminary findings indicating that STN neurons were sensitive not only to rewards obtained during task performance, but also to the expectation of reward when its delivery was delayed in time. Most of the modulations at the onset of reaching movement were combined with modulations following reward delivery, suggesting the convergence of signals related to the animal's movement and its outcome in the same neurons. Some neurons were also influenced by the visuomotor contingencies of the task, i.e., target location and/or movement direction. In addition, modulations were observed under conditions where reward delivery was not contingent on an instrumental response, even in the absence of a reward predictive cue. Taken as a whole, these results demonstrate a potential contribution of the STN to motivational control of behavior in the non-human primate, although problems in distinguishing neuronal signals related to reward from those related to motor behavior should be considered. Characterizing the specificity of reward processing in the STN remains challenging and could have important implications for understanding the influence of this key component of basal ganglia circuitry on emotional and motivated behaviors under normal and pathological conditions.
    Frontiers in Computational Neuroscience 12/2013; 7:175. DOI:10.3389/fncom.2013.00175 · 2.20 Impact Factor
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    • "Topography at the extremities is likely to be conserved if the proximal inputs, originating predominantly from one frontal area, remain more efficient than those more distal, as expected from the decremental propagation of the signal along the dendritic tree. Subregional specificity is not supported by electrophysiological data in monkeys, showing that STN neurons respond to stimuli predictive of reward or reward itself independently of their location within the nucleus (Darbaky et al., 2005) but this remains to be investigated for other functions subserved by the prefrontal cortex. "

    Frontiers in Computational Neuroscience 10/2013; 7:135. DOI:10.3389/fncom.2013.00135 · 2.20 Impact Factor
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