Academic journal article Cognitive, Affective and Behavioral Neuroscience

Genetic Polymorphisms of the Dopamine and Serotonin Systems Modulate the Neurophysiological Response to Feedback and Risk Taking in Healthy Humans

Academic journal article Cognitive, Affective and Behavioral Neuroscience

Genetic Polymorphisms of the Dopamine and Serotonin Systems Modulate the Neurophysiological Response to Feedback and Risk Taking in Healthy Humans

Article excerpt

Published online: 19 July 2012

© The Author(s) 2012. This article is published with open access at Springerlink.com

Abstract Genetic differences in the dopamine and serotonin systems have been suggested as potential factors underlying interindividual variability in risk taking and in brain activation during the processing of feedback. Here, we studied the effects of dopaminergic (dopamine transporter [DAT1], catecholamine-O-methyltransferase val158met [COMT]) and serotonergic (serotonin transporter [5HTTLPR]) polymorphisms on risk taking and brain responses following feedback in 60 healthy female subjects. The subjects completed a well-established experimental gambling paradigm while an electroencephalogram was recorded. During the task, risk-taking behavior and prefrontal brain responses (feedback-related negativity [FRN]) following monetary gains and losses were assessed. FRN amplitudes were enhanced for nine-repeat-allele carriers of the DAT1 and short-allele carriers of 5HTTLPR, which are both presumably linked to less transporter activity and higher neurotransmitter levels. Moreover, nine-repeat DAT1 carriers displayed a trend toward increased risk taking in general, whereas 5HTTLPR short-allele carriers showed decreased risk taking following gains. COMT val158met genotype was unrelated to FRN amplitude and average risk taking. However, COMT met/met carriers showed a pronounced feedback P3 amplitude independent of valence, and a gradual increase in risk taking during the gambling task. In sum, the present findings underline the importance of genetic variability in the dopamine and serotonin systems regarding the neurophysiology of feedback processing.

Keywords Dopamine . Serotonin . EEG . Feedback . Reward . Risk taking . DAT . 5HTTLPR . COMT

The neural mechanisms underlying action outcome evaluation are essential for flexible adaptation of behavior, and they are related to interindividual variability in risk-taking behavior. Part of this variance has been attributed to differences within the dopamine (DA) and the serotonin (5HT) systems (Jocham & Ullsperger, 2009). Holroyd and Coles (2002) put forward an influential theory regarding the neuroanatomical and neurochemical locus of performance monitoring and feedback processing. Their account is based on studies in primates (Montague, Hyman, & Cohen, 2004; Schultz, 2002) that showed an increase in mesencephalic DA firing if an outcome is better than expected (such as a correct response or reward) and ceasing of DA neuron firing if an outcome is worse than expected (such as an error or nonreward). According to Holroyd and Coles, such reward prediction errors are conveyed by the human midbrain DA system. Moreover, they argued that these transient DA dips are projected to frontal cortical areas, among them the anterior cingulate cortex (ACC). In the ACC, these prediction error signals disinhibit cortical pyramidal neurons, which in turn serve to adapt subsequent behavior.

Electrophysiological studies in humans have shown that the ACC activity caused by this prediction error manifests itself as a negative deflection in activity peaking at frontocentral scalp sites. This negativity was found after an erroneous response was made and was termed the "error-related negativity" (ERN; Gehring, Goss, Coles, Meyer, & Donchin, 1993). It has also been found after external feedback was given that signaled an error or nonreward (feedback-related negativity, or FRN; Gehring et al., 1993; Gehring & Willoughby, 2002; Nieuwenhuis, Holroyd, Mol, & Coles, 2004; Potts, Martin, Kamp, & Donchin, 2011). Studies on the FRN have been consistent in showing that its magnitude is sensitive to both negative feedback (Gehring & Willoughby, 2002; Hajcak, Moser, Holroyd, & Simons, 2006; Holroyd & Coles, 2002; Holroyd, Hajcak, & Larsen, 2006) and positive feedback (Holroyd & Krigolson, 2007). It is thought to reflect a learning signal, promoting the avoidance of behaviors that lead to bad outcomes (Holroyd & Coles, 2002; Nieuwenhuis et al. …

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