Encoding of Probabilistic Rewarding and Aversive Events by Pallidal and Nigral Neurons

Abstract

Previous studies have rarely tested whether the activity of high-frequency discharge (HFD) neurons of the basal ganglia (BG) is modulated by expectation, delivery, and omission of aversive events. Therefore the full value domain encoded by the BG network is still unknown. We studied the activity of HFD neurons of the globus pallidus external segment (GPe, n=310), internal segment (GPi, n=149), and substantia nigra pars reticulata (SNr, n=145) in two monkeys during a classical conditioning task with cues predicting the probability of food, neutral, or airpuff outcomes. The responses of BG HFD neurons were long-lasting and diverse with coincident increases and decreases in discharge rate. The population responses to reward-related events were larger than the responses to aversive and neutral-related events. The latter responses were similar, except for the responses to actual airpuff delivery. The fraction of responding cells was larger for reward-related events, with better discrimination between rewarding and aversive trials in the responses with an increase rather than a decrease in discharge rate. GPe and GPi single units were more strongly modulated and better reflected the probability of reward- than aversive-related events. SNr neurons were less biased toward the encoding of the rewarding events, especially during the outcome epoch. Finally, the latency of SNr responses to all predictive cues was shorter than the latency of pallidal responses. These results suggest preferential activation of the BG HFD neurons by rewarding compared with aversive events.

Temporal Convergence of Dynamic Cell Assemblies in the Striato-Pallidal Network

“…3b). This persistent GPe versus transient TANs response is expected from neurons along the BG main axis compared with neuromodulators and in line with previous observations (Joshua et al, 2008(Joshua et al, , 2009b. Next, we examined the average response of the low-frequency discharge MSNs and found it was also sustained (Fig.…”

“…Nevertheless, striatal MSNs are predicted to display sustained activity. This would correspond to their functional role in the BG network and previous observations of the GPe and BG output nuclei (Arkadir et al, 2004;Wichmann and Kliem, 2004;Joshua et al, 2009b).…”

“…Figure 3 displays the average response of all three populations to the presentation of the visual cues. GPe high-frequency discharge neurons increased and decreased their firing rates to cue presentation; we therefore averaged over the absolute response (Joshua et al, 2009b) and obtained an average sustained response that lasted throughout the entire 2 s of cue presentation (Fig. 3a).…”

“…The neuromodulators, specifically midbrain dopaminergic neurons and striatal cholinergic interneurons, display a homogeneous transient response, thus providing the main axis with a single-dimensional teaching message (Schultz, 1998;Bar-Gad et al, 2003;Joshua et al, 2008). Neurons in the main axis, however, specifically in the globus pallidus external segment (GPe) and the BG output structures, exhibit diverse activity with an average sustained response that enables a large information capacity (Mink, 1996;Bar-Gad et al, 2003;Joshua et al, 2009b). Possibly these long duration responses are similar to the set-related activity described in the cortex (Kojima and Goldman Rakic, 1982;Miyashita, 1988;Wise and Kurata, 1989;Funahashi et al, 1993;Fuster, 1999;Romo et al, 1999), which has been attributed to action preparation processes.…”

Pallidal spiking activity reflects learning dynamics and predicts performance

“…However, the role of the GPe in basic cognitive functions, in which the motor aspect plays a minor, marginal part and is not inherent to the task, has rarely been addressed directly (18), nor has its contribution in the context of actor-critic models.…”