The influence of personality on neural mechanisms of observational fear and reward learning

Abstract

Fear and reward learning can occur through direct experience or observation. Both channels can enhance survival or create maladaptive behavior. We used fMRI to isolate neural mechanisms of observational fear and reward learning and investigate whether neural response varied according to individual differences in neuroticism and extraversion. Participants learned object-emotion associations by observing a woman respond with fearful (or neutral) and happy (or neutral) facial expressions to novel objects. The amygdala-hippocampal complex was active when learning the object-fear association, and the hippocampus was active when learning the object-happy association. After learning, objects were presented alone; amygdala activity was greater for the fear (vs. neutral) and happy (vs. neutral) associated object. Importantly, greater amygdalahippocampal activity during fear (vs. neutral) learning predicted better recognition of learned objects on a subsequent memory test. Furthermore, personality modulated neural mechanisms of learning. Neuroticism positively correlated with neural activity in the amygdala and hippocampus during fear (vs. neutral) learning. Low extraversion/high introversion was related to faster behavioral predictions of the fearful and neutral expressions during fear learning. In addition, low extraversion/high introversion was related to greater amygdala activity during happy (vs. neutral) learning, happy (vs. neutral) object recognition, and faster reaction times for predicting happy and neutral expressions during reward learning. These findings suggest that neuroticism is associated with an increased sensitivity in the neural mechanism for fear learning which leads to enhanced encoding of fear associations, and that low extraversion/high introversion is related to enhanced conditionability for both fear and reward learning.

Personality traits modulate subcortical and cortical vestibular and anxiety responses to sound-evoked otolithic receptor stimulation

“…In previous imaging studies using resting-state measures in healthy volunteers, introversion was not associated with amygdala activity [78]. However, during emotional learning tasks, increased amygdala activity and high introversion were associated with enhanced fear conditioning and reward learning [81]. The increased amygdala response to vestibular stimuli in introverted subjects may thus support the hypothesis that conditioned hypersensitivity to vestibular stimuli plays a role in developing CSD [2].…”

Neural Correlates of Emotional Memories: A Review of Evidence From Brain Imaging Studies

“…Regarding the relationship between individual differences in both general emotion processing and specifically linked to emotional memory and brain activity, recent neuroimaging studies have shown that personality traits, such as extraversion and neuroticism, influence the neural correlates of emotion processing across a range of emotional processes, including experience, perception, attention, and memory (Canli, Sivers, Whitfield, Gotlib, & Gabrieli, 2002;Hamann & Canli, 2004;Hooker, Verosky, Miyakawa, Knight, & D'Esposito, 2008;Touryan et al, 2007). It has also been suggested that individual differences in emotional biases linked to personality might be rooted in an attentional network driven primarily by the AMY reactivity during the encoding of emotional stimuli (Haas & Canli, 2008).…”

“…It has also been suggested that individual differences in emotional biases linked to personality might be rooted in an attentional network driven primarily by the AMY reactivity during the encoding of emotional stimuli (Haas & Canli, 2008). Moreover, Hooker et al (2008) reported that activity in AMY and HC correlate with the level of neuroticism, during fear learning. These findings suggest that neuroticism, which has also been linked to vulnerability to affective disorders (Bienvenu et al, 2004), is associated with an increased sensitivity in the AMY and HC leading to enhanced encoding of negative associations.…”

Observational Fear Learning

“…Expressions of fear in a conspecific can serve as an effective US and engage fear-learning circuitry even when the source of fear in another is unknown (Hooker, Verosky, Miyakawa, Knight, & D'esposito, 2008). In one neuroimaging study, participants were presented with a series of novel objects paired with a fearful or neutral facial expression.…”

“…For example, personality traits such as neuroticism were shown to correlate positively with amygdala activity during observational fear learning (Hooker et al, 2008). Genetic variation in neurotransmitters known to modulate emotional learning and regulation also increases receptiveness to socially acquired fear.…”