Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories

Abstract

Learning to perform a behavioural procedure as a well-ingrained habit requires extensive repetition of the behavioural sequence, and learning not to perform such behaviours is notoriously difficult. Yet regaining a habit can occur quickly, with even one or a few exposures to cues previously triggering the behaviour. To identify neural mechanisms that might underlie such learning dynamics, we made long-term recordings from multiple neurons in the sensorimotor striatum, a basal ganglia structure implicated in habit formation, in rats successively trained on a reward-based procedural task, given extinction training and then given reacquisition training. The spike activity of striatal output neurons, nodal points in cortico-basal ganglia circuits, changed markedly across multiple dimensions during each of these phases of learning. First, new patterns of task-related ensemble firing successively formed, reversed and then re-emerged. Second, task-irrelevant firing was suppressed, then rebounded, and then was suppressed again. These changing spike activity patterns were highly correlated with changes in behavioural performance. We propose that these changes in task representation in cortico-basal ganglia circuits represent neural equivalents of the explore-exploit behaviour characteristic of habit learning.

Hierarchical recruitment of phasic dopamine signaling in the striatum during the progression of cocaine use

“…Consistent with our findings, dorsal striatal circuits serve to evaluate behavior and to exploit optimal behaviors following initial behavioral variability during trial-and-error learning (exploration) (35) as an integral part of the sensorimotor domain of the basal-ganglia network mediating action sequencing as well as selection/inhibition of competing motor programs (34,36). Thus, our findings suggest that the observed changes in DLS dopamine signaling (i.e., task representation in DLS circuits) might facilitate a switch from exploring the availability of drug rewards present in the environment to exploiting this environment.…”

Reversible online control of habitual behavior by optogenetic perturbation of medial prefrontal cortex

“…We used a navigational Tmaze task (Fig. 1A) similar to one developed to examine neural activity in the striatum during habit formation (13)(14)(15). We tracked the learning curves of multiple sets of rat subjects (n = 10).…”

Affective neuroscience of pleasure: reward in humans and animals

“…This alternative draws on the distinction between phasic dopamine signals (spike-triggered release limited to within synapses) and tonic dopamine signals (spike-independent release extending outside synapses) and typically assigns a learning role specifically to phasic signals (Grace 1991;Grace et al 2007;Niv et al 2007;Phillips et al 2003;Schultz 1997;. Learning and prediction roles of dopamine have been conceptualized as teaching signals, S-S prediction signals about future rewards, and S-R stamping-in or habit reinforcement ( Schultz et al 1997;Tobler et al 2005) and by target systems in nucleus accumbens and related forebrain structures (Aldridge et al 1993;Barnes et al 2005;Carelli 2004;Cromwell et al 2005;Day and Carelli 2007;Ghitza et al 2004;Roitman et al 2005;Taha and Fields 2006;Tindell et al 2004;Wan and Peoples 2006).…”