Signaling patterns of globus pallidus internal segment neurons during forearm rotation

Abstract

We recorded extracellular single unit discharges of globus pallidus internal segment (GPi) neurons in monkeys performing a visually-driven forearm rotation movement task in order to quantify how discharge patterns changed in relation to kinematic parameters. Subjects grasped a handle that rotated about its axis while facing a video screen displaying visual targets. Continuous visual feedback of handle rotation position was provided. Monkeys generated forearm rotation movements of ±35° and ±70° amplitude in order to align the cursor and targets. Trial records were aligned to forearm rotation onset in order to compare the discharge patterns that were associated with movements of different amplitudes, velocities, and directions. In addition, we quantified the depth of modulation of neuronal discharge associated with movements generated in two different task phases. Comparisons of discharge patterns were made between the visually-guided, rewarded phase ("cued movements") and the self-paced, unrewarded phase that returned the monkey to the task start position ("return movements") by quantifying the goodness of fit between neuronal discharge during cued and return movements.Our analyses revealed no systematic relationship between the depth of modulation of GPi neurons and forearm rotation amplitude, direction, or velocity. Further, comparisons between the two behavioral contexts revealed a systematic attenuation of modulation that could not be attributed to differences in movement velocity. Collectively, these findings suggest that the GPi neurons that we studied were not significantly involved in mediating movement kinematics, but may have instead been instrumental in the processing of information about the behavioral context during which movements were generated.

The encoding of cocaine vs. natural rewards in the striatum of nonhuman primates: categories with different activations

“…Other distinguishing features between DStr and VStr included differences in baseline firing rates (Figure 3–Figure 7), absence of prolonged discharge during intravenous cocaine delivery in DStr cells (Figure 7, Reward-Both ), and reduced sensitivity of VStr Cocaine-specific and Juice-specific cell firing to Nogotarget events (Figure 4&Figure 8). Such differences support prior and current proposals of an underlying scheme in which dorsal and ventral striatum provide differential encoding of reward contingent motor responses (Apicella et al 1991, Rebec 2006, Gdowski et al 2007, Atallah et al 2007, Takahashi et al 2007, Seger 2008). …”

Striatal and Pallidal Activation during Reward Modulated Movement Using a Translational Paradigm

“…Second, both striatal and pallidal regions displayed a greater response to financial gains compared to neutral outcomes. Our finding of context dependent modulation of basal ganglia response converges with the pallidal results reported by Gdowski and colleagues (2007; 2001) in monkey and with the role of the dorsal striatum in reward and decision-making described in the model by Balleine and colleagues (2007). Overall, these finding support the notion of a broader effect of context dependent modulation within subregions of the basal ganglia.…”

“…For example, nonhuman primate studies of reward outcome typically involve events that predict feedback, such as a tone indicating the animal should approach a target to receive a reward, but they may also include events that predict no feedback, such as a tone indicating the animal should return to the starting position in preparation for the next trial (Gdowski, Miller, Bastianen, Nenonene, & Houk, 2007). …”

“…These differences in response requirements between human and animal reward processing studies might explain why neurons in the dorsal striatum (comprised of the caudate nucleus and putamen) are often found to be responsive during movements elicited by reward cues in animal studies (Hollerman, Tremblay, & Schultz, 1998; Kawagoe, Takikawa, & Hikosaka, 1998), whereas the ventral striatum is often activated in human fMRI studies of reward cuing (Delgado, Miller, Inati, & Phelps, 2005; Galvan et al, 2005; Jensen et al, 2007; Knutson, et al, 2001). Differences in response requirements might also explain why some studies of reward-cued movement in non-human primates have found neurons in the internal globus pallidus, outside of the ventral pallidum, that discharge during reward-cued capture-movements (Gdowski, et al, 2007; Gdowski, Miller, Parrish, Nenonene, & Houk, 2001). Single cell recording data support the view that the basal ganglia are involved in setting movement parameters, thus contributing to movement control (DeLong et al, 1984; Evarts & Wise, 1984).…”

The human subthalamic nucleus and globus pallidus internus differentially encode reward during action control

“…Certain GPi neurons in the monkey project to the lateral habenula (LHb), a known limbic structure, and these neurons appear to encode reward prediction [Hong and Hikosaka, ; Matsumoto and Hikosaka, ]. A study of individual neuron behavior in monkeys performing reward‐motivated limb movements identified a population of GPi neurons that modulated firing rate in response to reward delivery [Gdowski et al, ]. These findings have recently been corroborated in humans.…”