Abstract
Previous studies have shown that appetitive motivation enhances episodic memory formation via a network including the substantia nigra/ventral tegmental area (SN/VTA), striatum and hippocampus. This functional magnetic resonance imaging (fMRI) study now contrasted the impact of aversive and appetitive motivation on episodic long-term memory. Cue pictures predicted monetary reward or punishment in alternating experimental blocks. One day later, episodic memory for the cue pictures was tested. We also investigated how the neural processing of appetitive and aversive motivation and episodic memory were modulated by dopaminergic mechanisms. To that end, participants were selected on the basis of their genotype for a variable number of tandem repeat polymorphism of the dopamine transporter (DAT) gene. The resulting groups were carefully matched for the 5-HTTLPR polymorphism of the serotonin transporter gene. Recognition memory for cues from both motivational categories was enhanced in participants homozygous for the 10-repeat allele of the DAT, the functional effects of which are not known yet, but not in heterozygous subjects. In comparison with heterozygous participants, 10-repeat homozygous participants also showed increased striatal activity for anticipation of motivational outcomes compared to neutral outcomes. In a subsequent memory analysis, encoding activity in striatum and hippocampus was found to be higher for later recognized items in 10-repeat homozygotes compared to 9/10-repeat heterozygotes. These findings suggest that processing of appetitive and aversive motivation in the human striatum involve the dopaminergic system and that dopamine plays a role in memory for both types of motivational information. In accordance with animal studies, these data support the idea that encoding of motivational events depends on dopaminergic processes in the hippocampus.
Highlights
Reward improves episodic memory formation in humans (Shohamy & Adcock, 2010)
The reverse contrasts revealed no significantly higher activations in heterozygotes compared homozygotes. These results suggest that the dopaminergic system is involved in the neural processing of appetitive and aversive motivation in humans and in memory formation for motivational stimuli
The main findings of the current study are (i) that anticipation of monetary punishments enhances long-term memory for punishment-predictive items, (ii) that dopamine genotype modulates recognition memory for motivational stimuli, and (iii) that dopamine genotype modulates striatal activity to reward and punishment anticipation and striatal and hippocampal activity related to subsequent memory for motivational items
Summary
Reward improves episodic memory formation in humans (Shohamy & Adcock, 2010). Functional imaging studies have shown that memory encoding of reward-associated stimuli involves a network of dopaminergic midbrain areas, ventral striatum and hippocampus Evidence from animal studies suggests that this reward-related modulation of long-term memory could be mediated by dopamine release in the hippocampus (Bethus, Tse, & Morris, 2010; for a review of dopamine effects on hippocampal longterm potentiation, see Lisman, Grace, & Duzel, 2011; Otmakhova, Duzel, Deutch, & Lisman, 2013; Rossato, Bevilaqua, Izquierdo, Medina, & Cammarota, 2009) This is supported by studies in humans indicating that dopamine binding potential in the hippocampus is correlated with memory performance (Backman et al, 2000; Cervenka, Backman, Cselenyi, Halldin, & Farde, 2008; Takahashi et al, 2007, 2008). When monetary rewards and punishments were dependent on memory performance, threat of monetary loss enhanced source memory retrieval in a similar manner to reward when tested immediately after learning (Shigemune, Tsukiura, Kambara, & Kawashima, 2013) This was associated with a correlation of activity in striatum and hippocampus during successful source retrieval. Increased dopaminergic transmission was expected to lead to improved episodic memory performance
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