Responses of Tonically Active Neurons in the Monkey Striatum Discriminate between Motivationally Opposing Stimuli

Abstract

The striatum is involved in the control of appetitively motivated behavior. We found previously that tonically active neurons (TANs) in the monkey striatum show discriminative responses to different stimuli that are appetitive or aversive. However, these differential responses may reflect the sensory qualities of the stimulus rather than its motivational value. In the present study, we sought to define more precisely the relationship between the particular aspect of the response of TANs and the motivational value of stimuli. For this purpose, three monkeys were presented with two types of aversive stimuli (loud sound and air puff) and one appetitive stimulus (fruit juice). In most instances, the TAN responses to the loud sound and the air puff were similar, in terms of response pattern and duration, whereas responses to the liquid reward showed distinct features. Using classical appetitive conditioning, we reversed the motivational value of a stimulus so that a previously aversive stimulus was now associatively paired with a reward and found that this manipulation selectively modifies the expression of TAN responses to the stimulus. These data indicate that the characteristics of neuronal responses undergo modifications when the valence of the stimulus is changed from aversive to appetitive during associative learning, suggesting that TANs may contribute to a form of stimulus encoding that is dependent on motivational attributes. The adaptation of TAN responses such as observed in the present study likewise reflects a neuronal system that adjusts to the motivational information about environmental events.

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).…”

An fMRI study of reward-related probability learning

“…The striatum can be subdivided into a dorsal (primarily caudate and putamen) and a ventral (primarily nucleus accumbens) components. Although more reward-related neurons are found in the ventral striatum (Apicella et al, 1991), research also suggests that some neurons in the dorsal striatum, specifically the caudate, also respond to reward (Kawagoe et al, 1998(Kawagoe et al, , 2004Lauwereyns et al, 2002;Ravel et al, 2003;Takikawa et al, 2002;Watanabe et al, 2003). This is supported by neuroimaging studies implicating the dorsal striatum in processing an array of rewards and punishments, such as money Delgado et al, 2000Delgado et al, , 2003Delgado et al, , 2004Elliott et al, 2000Elliott et al, , 2004Knutson et al, 2001aKnutson et al, , 2001b, liquids and odors (Berns et al, 2001;Gottfried et al, 2002;O'Doherty et al, 2002O'Doherty et al, , 2003O'Doherty et al, , 2004.…”

Tonically Active Neurons in the Primate Caudate Nucleus and Putamen Differentially Encode Instructed Motivational Outcomes of Action

“…This could also be the reason that, in previous studies, TANs responded selectively to reward-associated stimuli such as the click noise of a solenoid valve to deliver liquid reward, or selectively to reward itself when immediately followed by conditioned orofacial movement (Kimura et al, 1984;Apicella et al, 1991;Aosaki et al, 1994bAosaki et al, , 1995Ravel et al, 1999). Ravel et al (2003) recently reported that TANs discriminate between reward and no-reward (airpuff and loud sound) stimuli in terms of the temporal pattern of responses. The present study did not show a differential temporal pattern in the responses to outcome-associated instructions but did show a difference in the temporal response patterns between the instruction responses and GO responses (Figs.…”

“…Tonically active neurons (TANs), presumed cholinergic interneurons in the striatum (Wilson et al, 1990;Aosaki et al, 1995;Kawaguchi et al, 1995), were initially characterized by the responses to reward-associated stimuli (Kimura et al, 1984;Apicella et al, 1991;Kimura, 1992;Raz et al, 1996), by the evolution of responses via behavioral learning (Aosaki et al, 1994b), and by the involvement of the nigrostriatal dopaminergic system in the responses (Aosaki et al, 1994a). It was subsequently shown that TANs respond not only to reward-associated stimuli but also to aversive stimuli such as an airpuff on the face (Ravel et al, 1999;Blazquez et al, 2002;Ravel et al, 2003). Furthermore, the responses of TANs in the caudate nucleus to visual cues for eye movement tasks were selective to the contralateral visual field but much less selective to whether the cue was associated with reward or no-reward outcome (Shimo and Hikosaka, 2001).…”