The Role of Striatum in Initiation and Execution of Learned Action Sequences in Rats

Abstract

To understand the role of striatum in motor sequence learning, we trained rats to perform a series of tasks measuring speed and accuracy of responding to luminance cues presented as discriminative stimuli for single nose pokes or for sequences of nose pokes in a serial reaction time task. Habit (stimulus-response) learning was measured by comparing performances when stimuli were repeated (predictable) with when they were selected randomly (unpredictable). Sequences had defined start and end points and were limited to five nose pokes to minimize chunking. When sequences were repeated, response time (RT) increased for nose pokes initiating the sequence and decreased for nose pokes completing it. These effects developed incrementally across sessions, consistent with the time course of habit learning. Medial (mCPu), lateral, and complete (CPu) caudate-putamen lesions affected speed and accuracy of single nose poke responses, confirming the role of these areas in guiding responses with external sensory stimuli. None of these lesions affected the short-term increase in accuracy observed when single nose poke responses were repeated. Both mCPu and CPu lesions increased RTs for initiating sequential responses, effects that were exacerbated across sessions in which specific sequences were repeated. None of the lesions affected the gradual decrease in RT for nose pokes completing repeated sequences. Correlational analyses confirmed the relationship between the extent of dorsal striatal damage and the ability to respond to brief luminance cues and to initiate learned sequences. These results provide evidence implicating dorsal striatum in higher-level organizational aspects of learning reflected in planning that precedes the execution of learned action sequences.

The Role of the Striatum in Compulsive Behavior in Intact and Orbitofrontal-Cortex-Lesioned Rats: Possible Involvement of the Serotonergic System

“…The possibility that the striatum is mediating compulsive lever-pressing is in line with evidence implicating the striatum in the pathophysiology of OCD (for review see Stein, 2000) and with views on the central role of the striatum in habitual and compulsive behavior (Graybiel, 1998;Yin et al, 2004;Balleine, 2005;Everitt and Robbins, 2005;Bailey and Mair, 2006;Packard et al, 1989), although the latter have typically been related to the lateral, rather than medial, striatum. Furthermore, although the extrapolation from an animal model to the clinical condition is problematic and should be made with great caution, the results of this study support the possibility that in a subpopulation of OCD patients a primary pathology of the OFC leads to a dysregulation of the striatal serotonergic system that is manifested in compulsive behavior, and that antiobsessional/anticompulsive drugs exert their effects, in these patients, by normalizing the dysfunctional striatal serotonergic system (Joel et al, 2005a).…”

Inactivation of the Lateral But Not Medial Dorsal Striatum Eliminates the Excitatory Impact of Pavlovian Stimuli on Instrumental Responding

“…As such, it is not surprising that multiple neural structures contribute to the generation of PIT effects (Corbit and Balleine, 2005;Corbit et al, 2001;Hall et al, 2001;Murschall and Hauber, 2006). Previous findings have emphasized a role for the dorsal striatum in the acquisition of stimulus-reward (Aosaki et al 1994) and stimulus-response associations (Jog et al, 1999;Brasted and Wise, 2004;Yin et al, 2004;Barnes et al, 2005) and in stimulusguided performance (Kawagoe et al, 1998;Tremblay et al, 1998;Adams et al, 2001;Hassani et al, 2001;Cromwell and Schultz, 2003;Samejima et al, 2005;Bailey and Mair, 2006). These findings suggest that conditioned stimuli may direct instrumental behavior through dorsal striatal circuitry.…”

Modulation of Behavior by Expected Reward Magnitude Depends on Dopamine in the Dorsomedial Striatum

“…There is a considerable body of evidence that implicated the dorsal striatum in the acquisition of cue-reward associations (Aosaki et al 1994) and in cue-guided performance (Adams et al 2001;Bailey and Mair 2006;Hassani et al 2001;Kawagoe et al 1998;Samejima et al 2005;Tremblay et al 1998). For example, the neuronal activity of striatal neurons is influenced depending on the reward magnitude signaled in advance by discriminative cues (Cromwell and Schultz 2003) and plays a critical role in maintaining reward magnitude representations to guide actions (e.g., Hikosaka et al 2006).…”

“…Considerable evidence suggests that the dorsal striatum is important in mediating the impact of reward-predictive stimuli on behavior. For example, electrophysiological studies demonstrated that the dorsal striatum is involved in the acquisition of stimulus-reward (Aosaki et al 1994) and stimulus-response associations (Barnes et al 2005;Brasted and Wise 2004;Jog et al 1999;Yin and Knowlton 2004) as well as in stimulus-guided performance (Adams et al 2001;Bailey and Mair 2006;Cromwell and Schultz 2003;Hassani et al 2001;Kawagoe et al 1998;Samejima et al 2005;Tremblay et al 1998). Different subregions of the dorsal striatum play distinct roles in the modulation of behavior by reward-predictive cues.…”