The Role of Striatal Tonically Active Neurons in Reward Prediction Error Signaling during Instrumental Task Performance

Abstract

The detection of differences between predictions and actual outcomes is important for associative learning and for selecting actions according to their potential future reward. There are reports that tonically active neurons (TANs) in the primate striatum may carry information about errors in the prediction of rewards. However, this property seems to be expressed in classical conditioning tasks but not during performance of an instrumental task. To address this issue, we recorded the activity of TANs in the putamen of two monkeys performing an instrumental task in which probabilistic rewarding outcomes were contingent on an action in block-design experiments. Behavioral evidence suggests that animals adjusted their performance according to the level of probability for reward on each trial block. We found that the TAN response to reward was stronger as the reward probability decreased; this effect was especially prominent on the late component of the pause-rebound pattern of typical response seen in these neurons. The responsiveness to reward omission was also increased with increasing reward probability, whereas there were no detectable effects on responses to the stimulus that triggered the movement. Overall, the modulation of TAN responses by reward probability appeared relatively weak compared with that observed previously in a probabilistic classical conditioning task using the same block design. These data indicate that instrumental conditioning was less effective at demonstrating prediction error signaling in TANs. We conclude that the sensitivity of the TAN system to reward probability depends on the specific learning situation in which animals experienced the stimulus-reward associations.

Differential Effects of Systemic Cholinergic Receptor Blockade on Pavlovian Incentive Motivation and Goal-Directed Action Selection

“…This is consistent with numerous reports that tonically active interneurons (TANs) in the striatum, which are believed to be cholinergic, develop a characteristic pause-rebound firing pattern in response to reward-predictive stimuli (Apicella et al, 2011;Matsumoto et al, 2001;Ravel et al, 2003). Interestingly, task-related modulation of TAN firing appears to be more prominent during simple Pavlovian (stimulus-reward) conditioning than during cue-triggered instrumental (stimulus-response-reward) conditioning (Apicella et al, 2011). This is noteworthy because the Pavlovian-to-instrumental transfer task used here was designed to assay the influence of purely Pavlovian cues on reward seeking.…”

Cortical and Thalamic Excitation Mediate the Multiphasic Responses of Striatal Cholinergic Interneurons to Motivationally Salient Stimuli

“…The monkeys were seated in a restraining box that was described previously (Apicella et al, 1997) and faced a panel placed ϳ30 cm in front of them. Each was chronically fitted with a head-restraining device and a recording chamber over a craniotomy for electrode insertions mainly targeted at the putamen.…”

“…Each was chronically fitted with a head-restraining device and a recording chamber over a craniotomy for electrode insertions mainly targeted at the putamen. Surgical and electrophysiological procedures were as described previously (Apicella et al, 1997). Monkey surgery and behavioral testing protocols were in accordance with guidelines set by the National Institutes of Health and the French government regulations on animal experimentation.…”

“…Signals from neuronal activity were conventionally amplified, filtered (band pass, 0.3-1.5 kHz), and converted to digital pulses through a window discriminator. Putative cholinergic interneurons (TANs) were classified according to their electrophysiological characteristics, as described previously (Aosaki et al, 1994), as well as their typical responses to unexpected rewarding stimuli (Apicella et al, 1997). Our focus on TANs recorded in putamen was not only in keeping with many other past studies of salience-/reward-related TAN activity in behaving primates (Aosaki et al, 1994;Apicella et al, 1997;Morris et al, 2004), but also allowed for the most direct comparison (in terms of broadly equivalent circuits and function) with our sample of rat cholinergic interneurons.…”

“…Putative cholinergic interneurons (TANs) were classified according to their electrophysiological characteristics, as described previously (Aosaki et al, 1994), as well as their typical responses to unexpected rewarding stimuli (Apicella et al, 1997). Our focus on TANs recorded in putamen was not only in keeping with many other past studies of salience-/reward-related TAN activity in behaving primates (Aosaki et al, 1994;Apicella et al, 1997;Morris et al, 2004), but also allowed for the most direct comparison (in terms of broadly equivalent circuits and function) with our sample of rat cholinergic interneurons. Although there is some regional bias in the responses of primate striatal neurons to salient/rewarding stimuli, uniformity in TAN responses across the striatal axis has been commonly emphasized (Morris et al, 2004;Adler et al, 2013a;Adler et al, 2013b).…”