Contributions of the striatum to learning, motivation, and performance: an associative account

Abstract

It has long been recognized that the striatum is composed of distinct functional sub-units that are part of multiple cortico-striatal-thalamic circuits. Contemporary research has focused on the contribution of striatal sub-regions to three main phenomena: learning of associations between stimuli, actions and rewards; selection between competing response alternatives; and motivational modulation of motor behavior. Recent proposals have argued for a functional division of the striatum along these lines, attributing, for example, learning to one region and performance to another. Here, we consider empirical data from human and animal studies, as well as theoretical notions from both the psychological and computational literatures, and conclude that striatal sub-regions instead differ most clearly in terms of the associations being encoded in each region.

Figure 1

Schematic representation of corticostriatal connections based on [1,2,87,88]. Different cortical areas project to different sub-regions of the striatum, which then project back to respective cortical areas via the internal segment of the globus pallidus (GPi) and the thalamus (direct pathway). Not shown projections include those from different striatal sub-regions to distinct areas in the substantia nigra pars reticulata (SNr) and the external segment of the globus pallidus, as well as those from distinct midbrain nuclei (e.g., substantia nigra compacta and ventral tegmental area) to different striatal sub-regions. Moreover, in the ventral striatum, the Nacc shell, but not the core, projects heavily to the amygdala and lateral hypothalamus, whereas both the shell and core receive inputs from limbic regions (e.g., amygdala and hippocampus). Circle, inhibitory connection; Arrow, excitatory connection; DMS, dorsomedial striatum; DLS, dorsolateral striatum; GPi, internal segment of globus pallidus; VP, ventral pallidum; VA, ventral anterior; DM, dorsomedial; VL, ventrolateral; VM, ventromedial; Nacc C, nucleus accumbens core; Nacc Sh, nucleus accumbens shell.

Figure 2

Human neuroimaging studies that indicate differential contributions of striatal sub-regions in associative encoding. (a) Striatal activity tracking the development of habits in posterior lateral striatum (top) and during goal-directed instrumental performance in anterior DMS (bottom). Reproduced, with permission, from [23] and [22], respectively. (b) Activity in the lateral striatum (top) as participants executed a well-trained motor sequence and in the DMS (bottom) as participants planned performance of a self-generated, novel, motor sequence. Reproduced, with permission, from [5]. No effects were found in the DMS when participants planned performance of a well-trained sequence (condition not shown here). (c) Effects in the VS (left) for the conjunction of high versus low incentives and correlation with performance levels. Activity in the lateral striatum is correlated with VS activity when the task entails high demands on motor performance (center), while activity in the medial striatum (right) correlates with the VS signal during high demands on cognitive performance. Reproduced, with permission, from [13]. (d) Imaging effects in the lateral VS for specific PIT (left) and in the medial VS for general PIT (right). Reproduced, with permission, from [47] and [46] respectively. (e) BOLD responses in the VS in anticipation of monetary gain (left) and loss (right), with % signal change shown in bar graph on far right, for gain (blue), no outcome (gray), and loss (red). Reproduced, with permission, from [64].