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

Abstract

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-[18F]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 Kinapp). 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 may be driven by ventral striatal activation during reward-related learning, which in turn proved to be inversely associated with ventral striatal dopamine synthesis capacity.

The role of learning-related dopamine signals in addiction vulnerability

“…It is conceivable that reductions in presynaptic D 2 receptors might also affect tonic dopamine signals (Martinez et al, 2005(Martinez et al, , 2009 and that this relates to the effects of dopamine and cached values on Pavlovian-instrumental transfer (Murschall and Hauber, 2006;Wyvell and Berridge, 2000) and sign-tracking . There is also evidence that the link between dopamine synthesis and phasic prediction errors is altered by addiction, and this might be mediated by a failure of the presynaptic D 2 control (Schlagenhauf et al, 2013;Deserno et al, 2013). Moreover, Flagel et al (2010Flagel et al ( , 2013 have shown that selectively bred rats with a predisposition towards sign-tracking behaviour and addiction have lower levels of D 2 mRNA in the nucleus accumbens and dorsal striatum, but not in the ventral tegmental area.…”

Public mental health: a call to action

“…First, a series of animal experiments and human studies have shown that social stress factors, particularly exclusion, stigmatization and discrimination, directly impact on the neurobiological correlates of mental disorders, impair cognitive capacities and promote aggression, drug intake and negative mood states (4,5). Indeed, even fluid IQ as a measure of complex cognitive capacities has been associated with variation in dopaminergic neurotransmission, which in turn is strongly affected by stress exposure (6)(7)(8). Second, most twin research has relied on the (controversial) assumption that gene-gene interactions are only additive and cannot exponentially increase similarity (e.g., when variation in multiple genes increases neurotransmitter synthesis and at the same time decreases both reuptake and metabolism).…”

“…"Top-down" solutions (i.e., those developed by government experts) that are imposed on communities are often bureaucratic, reductionistic, overly prescriptive, and insensitive to local culture and context. The expensive and inefficient Veterans Administration Healthcare system in the U.S. is often cited as an example of the failure of top-down systems (6).…”

Altered reward anticipation: Potential explanation for weight gain in schizophrenia?

“…Schlagenhauf et al (2012) measured dopamine synthesis capacity, which is more closely related to tonic dopamine release than the shorter-lived dopamine release measures of Schott et al (2008). While Schott et al might have measured the faster phasic response, the DSC in Schlagenhauf et al's study is more related to the tonic dopamine release.…”

“…It is likely that dopamine synthesis capacity as indexed by DOPA is regulated by presynaptic autoreceptors. Accordingly, Schlagenhauf et al (2012) propose that the negative correlation between striatal dopamine synthesis capacity and prediction error-related activity may reflect the homeostatic role of autoreceptors. In contrast, raclopride-displacement as used by Schott and colleagues primarily reflects postsynaptic effects of dopamine release, implying a positive monotonic relation between striatal fMRI and raclopridedisplacement.…”