Regional specialization within the human striatum for diverse psychological functions

Decades of animal and human neuroimaging research have identified distinct, but overlapping, striatal zones, which are interconnected with separable corticostriatal circuits, and are crucial for the organization of functional systems. Despite continuous efforts to subdivide the human striatum based on anatomical and resting-state functional connectivity, characterizing the different psychological processes related to each zone remains a work in progress. Using an unbiased, data-driven approach, we analyzed large-scale coactivation data from 5,809 human imaging studies. We (i) identified five distinct striatal zones that exhibited discrete patterns of coactivation with cortical brain regions across distinct psychological processes and (ii) identified the different psychological processes associated with each zone. We found that the reported pattern of cortical activation reliably predicted which striatal zone was most strongly activated. Critically, activation in each functional zone could be associated with distinct psychological processes directly, rather than inferred indirectly from psychological functions attributed to associated cortices. Consistent with well-established findings, we found an association of the ventral striatum (VS) with reward processing. Confirming less well-established findings, the VS and adjacent anterior caudate were associated with evaluating the value of rewards and actions, respectively. Furthermore, our results confirmed a sometimes overlooked specialization of the posterior caudate nucleus for executive functions, often considered the exclusive domain of frontoparietal cortical circuits. Our findings provide a precise functional map of regional specialization within the human striatum, both in terms of the differential cortical regions and psychological functions associated with each striatal zone.In addition to its central role in selecting, planning, and executing motor behavior (1, 2), the human striatum has been reported to be involved in diverse psychological functions, including emotion generation and regulation (3, 4), reward-related processes and decision making (5, 6), and executive functions (7, 8). These discrete functions are thought to map onto distinct functional striatal zones, which participate in separable basal ganglia-thalamocortical circuits (9–12) and are critical for the organization of behavior.Following this logic, recent attempts to parcellate the human striatum using diffusion tensor imaging (DTI) (13, 14) and resting-state functional connectivity (RSFC) (15–17) have relied on patterns of corticostriatal connectivity to identify striatal zones. Although very useful, these studies have been limited to inferring striatal function indirectly via psychological functions of connected cortical regions. In addition, it remains unclear how anatomical connections and RSFC map onto different psychological processes (18). Finally, RSFC is sometimes epiphenomenal (19), and fiber tract reconstruction with DTI is inaccurate for complex axonal projections underlying frontal corticostriatal connectivity (17).A separate body of work has attempted to differentiate striatal contributions directly to behavior empirically. However, these empirical investigations have focused on a restricted set of paradigms that may fail to capture the full range of striatal function, especially in humans. For example, converging evidence suggests a division of labor between the ventral striatum (VS) and dorsal striatum for Pavlovian and instrumental conditioning, respectively (20, 21). Within the dorsal striatum, medial regions support behavioral flexibility and lateral regions support well-learned behavior (22, 23). This work has greatly advanced our understanding of the similarities of striatal function in human and nonhuman animals. However, because of this strong reliance on classic learning paradigms, the integration of ideas about how the striatum is involved in uniquely human psychological functions, such as working memory, planning, and language, remains a work in progress.To generate a comprehensive and precise functional map of the human striatum, in terms of associations with both cortical brain regions and psychological tasks, we simultaneously analyzed corticostriatal coactivation patterns and the frequency of psychological terms in the full text of 5,809 neuroimaging studies (24). In contrast to studies of RSFC, we defined corticostriatal associations based on coactivation in task-related responses across studies. A cortical voxel and a striatal voxel were coactivated if a study reported activation in both voxels. This metric groups voxels that are associated with similar psychological processes. Similar to RSFC, this metric does not imply direct functional coupling of coactivated voxels. In contrast to existing work, we attempted to associate psychological functions with striatal areas directly, rather than inferring them indirectly based on the psychological functions of connected cortical areas. Sampling across a broad spectrum of neuroimaging studies, without regard for the psychological process under investigation, allowed a large-scale comparison of associations of striatal subregions with diverse psychological processes. This data-driven approach allowed us to (i) localize five striatal zones based on their coactivation with cortical brain areas and (ii) simultaneously characterize the association of each zone with psychological states in a relatively unbiased manner, including potential associations overlooked in both individual hypothesis-driven studies and studies of RSFC.