Individual differences in emotion-cognition interactions: emotional valence interacts with serotonin transporter genotype to influence brain systems involved in emotional reactivity and cognitive control

Abstract

The serotonin transporter gene (5-HTTLPR) influences emotional reactivity and attentional bias toward or away from emotional stimuli, and has been implicated in psychopathological states, such as depression and anxiety disorder. The short allele is associated with increased reactivity and attention toward negatively-valenced emotional information, whereas the long allele is associated with increased reactivity and attention toward positively-valenced emotional information. The neural basis for individual differences in the ability to exert cognitive control over these bottom-up biases in emotional reactivity and attention is unknown, an issue investigated in the present study. Healthy adult participants were divided into two groups, either homozygous carriers of the 5-HTTLPR long allele or homozygous carriers of the short allele, and underwent functional magnetic resonance imaging (fMRI) while completing an Emotional Stroop-like task that varied in the congruency of task-relevant and task-irrelevant information and the emotional valence of the task-irrelevant information. Behaviorally, participants demonstrated the classic "Stroop effect" (responses were slower for incongruent than congruent trials), which did not differ by 5-HTTLPR genotype. However, fMRI results revealed that genotype influenced the degree to which neural systems were engaged depending on the valence of the conflicting task-irrelevant information. While the "Long" group recruited prefrontal control regions and superior temporal sulcus during conflict when the task-irrelevant information was positively-valenced, the "Short" group recruited these regions during conflict when the task-irrelevant information was negatively-valenced. Thus, participants successfully engaged cognitive control to overcome conflict in an emotional context using similar neural circuitry, but the engagement of this circuitry depended on emotional valence and 5-HTTLPR status. These results suggest that the interplay between emotion and cognition is modulated, in part, by a genetic polymorphism that influences serotonin neurotransmission.

Keywords: 5-HTTLPR; Stroop; anxiety; eye-gaze; fMRI; positive affect; prefrontal cortex (PFC).

Figure 1

Example stimuli for six conditions that varied by target direction to eye gaze (distractor) congruency and by emotional expression valence: (A) Happy/Congruent, (B) Happy/Incongruent, (C) Angry/Congruent, (D) Angry/Incongruent, (E) Neutral/Congruent, (F) Neutral/Incongruent.

Figure 2

Interaction between emotional valence and 5-HTTLPR for the interference contrast (incongruent > congruent) in four regions: (A) right dorsal lateral prefrontal cortex (R dlPFC); (B) left dorsal lateral prefrontal cortex (L dlPFC); (C) medial superior prefrontal cortex (BA 8); (D) left superior temporal sulcus (L STS). Graphs show mean contrast estimates (± standard error) in the activated cluster by genotype and emotional valence.

Figure 3

Regions in which increased activation for the contrast of incongruent—congruent trials correlates with (A) increased anxiety in Short 5-HTTLPR individuals viewing Angry faces (ventromedial prefrontal cortex and frontal pole); (B) increased trait positive affect in Long 5-HTTLPR individuals viewing Happy faces (bilateral ventral striatum).