Ventral striatal prediction error signaling is associated with dopamine synthesis capacity and fluid intelligence

Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité-Universitätsmedizin Berlin, Germany.
Human Brain Mapping (Impact Factor: 5.97). 06/2013; 34(6). DOI: 10.1002/hbm.22000
Source: PubMed


Fluid intelligence represents the capacity for flexible problem solving and rapid behavioral adaptation. Rewards drive flexible behavioral adaptation, in part via a teaching signal expressed as reward prediction errors in the ventral striatum, which has been associated with phasic dopamine release in animal studies. We examined a sample of 28 healthy male adults using multimodal imaging and biological parametric mapping with (1) functional magnetic resonance imaging during a reversal learning task and (2) in a subsample of 17 subjects also with positron emission tomography using 6-[(18) F]fluoro-L-DOPA to assess dopamine synthesis capacity. Fluid intelligence was measured using a battery of nine standard neuropsychological tests. Ventral striatal BOLD correlates of reward prediction errors were positively correlated with fluid intelligence and, in the right ventral striatum, also inversely correlated with dopamine synthesis capacity (FDOPA K inapp). When exploring aspects of fluid intelligence, we observed that prediction error signaling correlates with complex attention and reasoning. These findings indicate that individual differences in the capacity for flexible problem solving relate to ventral striatal activation during reward-related learning, which in turn proved to be inversely associated with ventral striatal dopamine synthesis capacity. Hum Brain Mapp, 2012. © 2012 Wiley Periodicals, Inc.

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Available from: Anthony Grace, Jan 07, 2014
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    • "The functional differentiation of specific striatal areas for cognition has been suggested before, for instance distinguishing between ventral (learning) and dorsal (response execution) regions [Humphries and Prescott, 2010; Mac- Donald et al., 2011; Schlagenhauf et al., 2013; Voorn et al., 2004; Wickens et al., 2007]. Here we report converging morphological evidence, given that we observed anteroventral , but virtually no caudal and dorsal areas of the basal ganglia, to be significantly relevant for cognitive performance. "
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    ABSTRACT: Neuroimaging studies have revealed associations between intelligence and brain morphology. However, researchers have focused primarily on the anatomical features of the cerebral cortex, whereas subcortical structures, such as the basal ganglia (BG), have often been neglected despite extensive functional evidence on their relation with higher-order cognition. Here we performed shape analyses to understand how individual differences in BG local morphology account for variability in cognitive performance. Structural MRI was acquired in 104 young adults (45 men, 59 women, mean age = 19.83, SD = 1.64), and the outer surface of striatal structures (caudate, nucleus accumbens, and putamen), globus pallidus, and thalamus was estimated for each subject and hemisphere. Further, nine cognitive tests were used to measure fluid (Gf), crystallized (Gc), and spatial intelligence (Gv). Latent scores for these factors were computed by means of confirmatory factor analysis and regressed vertex-wise against subcortical shape (local displacements of vertex position), controlling for age, sex, and adjusted for brain size. Significant results (FDR < 5%) were found for Gf and Gv, but not Gc, for the right striatal structures and thalamus. The main results show a relative enlargement of the rostral putamen, which is functionally connected to the right dorsolateral prefrontal cortex and other intelligence-related prefrontal areas. Hum Brain Mapp, 2013. © 2013 Wiley Periodicals, Inc.
    Human Brain Mapping 05/2014; 35(5). DOI:10.1002/hbm.22305 · 5.97 Impact Factor
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    • "This may point to a common biological alteration even in a heterogeneous population of schizophrenia patients. Theoretical work (Heinz, 2002; Kapur, 2003), and previous work in our group (Schlagenhauf et al., 2013), support the idea that VS hypoactivation in schizophrenia may be related to elevated levels of dopamine . Indeed, prediction error BOLD correlates are inversely correlated with dopamine synthesis capacity (measured by FDOPA PET) in the ventral striatum (Schlagenhauf et al., 2012). "
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    ABSTRACT: Subjects with schizophrenia are impaired at reinforcement-driven reversal learning from as early as their first episode. The neurobiological basis of this deficit is unknown. We obtained behavioral and fMRI data in 24 unmedicated, primarily first episode, schizophrenia patients and 24 age-, IQ- and gender-matched healthy controls during a reversal learning task. We supplemented our fMRI analysis, focusing on learning from prediction errors, with detailed computational modeling to probe task solving strategy including an ability to deploy an internal goal directed model of the task. Patients displayed reduced functional activation in the ventral striatum (VS) elicited by prediction errors. However, modeling task performance revealed that a subgroup did not adjust their behavior according to an accurate internal model of the task structure, and these were also the more severely psychotic patients. In patients who could adapt their behavior, as well as in controls, task solving was best described by cognitive strategies according to a Hidden Markov Model. When we compared patients and controls who acted according to this strategy, patients still displayed a significant reduction in VS activation elicited by informative errors that precede salient changes of behavior (reversals). Thus, our study shows that VS dysfunction in schizophrenia patients during reward-related reversal learning remains a core deficit even when controlling for task solving strategies. This result highlights VS dysfunction is tightly linked to a reward-related reversal learning deficit in early, unmedicated schizophrenia patients.
    NeuroImage 11/2013; 89(100). DOI:10.1016/j.neuroimage.2013.11.034 · 6.36 Impact Factor
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    • "NS3 appears more trait-like (evidenced by much higher test-rest correlation) than NS2 (Takeuchi et al., 2011), and appears to index those traits (irresponsibility, inability to approach life planfully) most strongly linked to general EXT risk (Krueger and South, 2009). It is particularly notable that only NS3 correlates with impaired decision-making on the Iowa Gambling Task (Álvarez-Moya et al., 2011), which has been linked to increased VS FDOPA KI values (Schlagenhauf et al., 2012). "
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    ABSTRACT: Impulse control disorders (ICDs), including disordered gambling, can occur in a significant number of patients with Parkinson's disease (PD) receiving dopaminergic therapy. The neurobiology underlying susceptibility to such problems is unclear, but risk likely results from an interaction between dopaminergic medication and a pre-existing trait vulnerability. Impulse control and addictive disorders form part of a broader psychopathological spectrum of disorders, which share a common underlying genetic vulnerability, referred to as externalizing. The broad externalizing risk factor is a continuously varying trait reflecting vulnerability to various impulse control problems, manifested at the overt level by disinhibitory symptoms and at the personality level by antecedent traits such as impulsivity and novelty/sensation seeking. Trait "disinhibition" is thus a core endophenotype of ICDs, and a key target for neurobiological investigation. The ventral striatal dopamine system has been hypothesized to underlie individual variation in behavioral disinhibition. Here, we examined whether individual differences in ventral striatal dopamine synthesis capacity predicted individual variation in disinhibitory temperament traits in individuals with PD. Eighteen early-stage male PD patients underwent 6-[F]Fluoro-l-DOPA (FDOPA) positron emission tomography scanning to measure striatal dopamine synthesis capacity, and completed a measure of disinhibited personality. Consistent with our predictions, we found that levels of ventral, but not dorsal, striatal dopamine synthesis capacity predicted disinhibited personality, particularly a propensity for financial extravagance. Our results are consistent with recent preclinical models of vulnerability to behavioral disinhibition and addiction proneness, and provide novel insights into the neurobiology of potential vulnerability to impulse control problems in PD and other disorders.
    Frontiers in Psychology 02/2013; 4:90. DOI:10.3389/fpsyg.2013.00090 · 2.80 Impact Factor
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