Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning

By Suzanne N. Haber, Ki-Sok Kim, P. Mailly, Roberta Calzavara. Journal of Neuroscience, 2006

709 citations recorded by the source corpus.

The anterior cingulate and orbital cortices and the ventral striatum process different aspects of reward evaluation, whereas the dorsolateral prefrontal cortex and the dorsal striatum are involved in cognitive function. Collectively, these areas are critical to decision making. We mapped the striatal area that receives information about reward evaluation. We also explored the extent to which terminals from reward-related cortical areas converge in the striatum with those from cognitive regions. Using three-dimensional-rendered reconstructions of corticostriatal projection fields along with two-dimensional chartings, we demonstrate the reward and cognitive territories in the primate striatum and show the convergence between these cortical inputs. The results show two labeling patterns: a focal projection field that consists of densely distributed terminal patches, and a diffuse projection consisting of clusters of fibers, extending throughout a wide area of the striatum. Together, these projection fields demonstrate a remarkably large, rostral, reward-related striatal territory that reaches into the dorsal striatum. Fibers from different reward-processing and cognitive cortical areas occupy both separate and converging territories. Furthermore, the diffuse projection may serve a separate integrative function by broadly disseminating general cortical activity. These findings show that the rostral striatum is in a unique position to mediate different aspects of incentive learning. Furthermore, areas of convergence may be particularly sensitive to dopamine modulation during decision making and habit formation.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/130140c850d4263ae254463b8569fe0b5b93f256

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Citations in the corpus

The Reward Circuit: Linking Primate Anatomy and Human Imaging (2010, methodology): “Taken together, the vmPFC, OFC, and dACC project primarily to the rostral striatum, with the vmPFC projecting most medially (to the NAcc) and the dACC most laterally (Haber et al , 2006), with the OFC terminal fields positioned between them.”
The feedback-related negativity (FRN) revisited: New insights into the localization, meaning and network organization (2014, background): “, 2007) or the striatum (Haber et al., 2006; Kunishio and Haber, 1994), several authors suggested that thedACC receives inputs from these areas to compare behavioral options and choose the optimal among them (Hare et al.”
Neurobiology of anorexia and bulimia nervosa. (2008, background): “The AVS and dorsal caudate are components of limbic and executive-associative pathways [94–96].”
The orbitofrontal cortex and beyond: from affect to decision-making. (2008, background): “…to the cingulate cortex (Carmichael and Price, 1996; Price, 2006), the ventral striatum (Ferry et al., 2000) and head of the caudate nucleus (Haber et al., 2006; Kemp and Powell, 1970), medial prefrontal cortex area 10 (Price, 2007), entorhinal and perirhinal cortex (Barbas, 2007; Insausti…”
Development of Large-Scale Functional Brain Networks in Children (2009, background): “These patterns support the parallel flow of cortical signals inputs into the basal ganglia, where multiple reward related signals are integrated in ways that facilitate incentive learning over short time scales and habit formation over long time scales [68,69].”
The role of the nucleus accumbens and rostral anterior cingulate cortex in anhedonia: Integration of resting EEG, fMRI, and volumetric techniques (2009, background): “It receives dense dopaminergic innervation (Gaspar et al., 1989) and projects to the striatum (in particular the NAcc) and the ventral tegmental area (Haber et al., 2006; Öngür and Price, 2000; Sesack and Pickel, 1992).”
Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia (2008, result): “Consistent with results from a recent invasive tracing study in primates (Haber et al., 2006), we demonstrate clearly defined striatal regions with overlap of connections with OFC, MPFC, or DLPFC (Figs.”
Multiple Forms of Value Learning and the Function of Dopamine (2009, positive): “Another brain region implicated in Pavlovian valuation is the ventral striatum, which receives afferent input from both the amygdala and orbitofrontal cortex (Fudge et al., 2002; Haber et al., 2006).”
Neuronal Reward and Decision Signals: From Theories to Data. (2015, background): “For neuronal decision models involving the basal ganglia, key features are the well-organized corticostriatal projections, internal connections, and parallel loops with cortex (7, 141, 164, 196, 197, 252); the synaptic convergence through the component structures (FIGURE 48B) (416, 430); the separat”
The cortico-basal ganglia integrative network: the role of the thalamus (2008, background): “Projections from the ACC/OFC terminate primarily in the rostral, ventro-medial striatum [6,24].”