Amygdala and hippocampus fail to habituate to faces in individuals with an inhibited temperament

Abstract

Habituation is a basic form of learning that reflects the adaptive reduction in responses to a stimulus that is neither threatening nor rewarding. Extremely shy, or inhibited individuals, are typically slow to acclimate to new people, a behavioral pattern that may reflect slower habituation to novelty. To test this hypothesis, we used functional magnetic resonance imaging to examine habituation to neutral faces in 39 young adults with either an extreme inhibited or extreme uninhibited temperament. Our investigation focused on two key brain regions involved in response to novelty—the amygdala and the hippocampus. Habituation to neutral faces in the amygdala and hippocampus differed significantly by temperament group. Individuals with an uninhibited temperament demonstrated habituation in both the amygdala and hippocampus, as expected. In contrast, in individuals with an inhibited temperament, the amygdala and hippocampus failed to habituate across repeated presentations of faces. The failure of the amygdala and hippocampus to habituate to faces represents a novel neural substrate mediating the behavioral differences seen in individuals with an inhibited temperament. We propose that this failure to habituate reflects a social learning deficit in individuals with an inhibited temperament and provides a possible mechanism for increased risk for social anxiety.

Amygdala habituation: A reliable fMRI phenotype

“…We calculated two different amygdala habituation indices: (1) the amplitude difference between the first and last stimulation block (FmL; Blackford et al, 2013) and (2) modeling of habituation by means of the regression (REG) approach.…”

“…Several studies have also demonstrated hemispheric lateralization with stronger habituation in the right versus left amygdala (Denny et al, in press;Lonsdorf et al, 2011;Phillips et al, 2001;Wedig et al, 2005;Wright et al, 2001). Of particular interest from the clinical perspective, amygdala habituation has been shown to be negatively correlated with trait anxiety (Hare et al, 2008), increased risk for social anxiety disorder (Blackford et al, 2013) and autism spectrum disorder (Kleinhans et al, 2009;Swartz et al, 2013;Wiggins et al,2014). Furthermore, it is sensitive to genetic variants linked to depression, anxiety, aggression and neuroticism (Fisher et al, 2009;Lonsdorf et al, 2011;Wiggins et al, 2014).…”

Processing of different types of social threat in shyness: Preliminary findings of distinct functional neural connectivity

“…fMRI studies employing "less threatening" social stimuli have demonstrated increased modulation of the dorsal (dACC) and superior temporal sulcus to faces with moderate emotional intensity and ambiguous faces, respectively, in shy adults (Tatham, Schmidt, Beaton, Schulkin, & Hall, 2013); and sustained amygdalar and hippocampal activation to neutral faces in a 2 TANG ET AL. group of extremely inhibited individuals, although some of them met criteria for social anxiety disorders (Blackford, Allen, Cowan, & Avery, 2013). Greater modulation of brain regions involved in attention, planning, and higher order visual processing have also been observed in individuals scoring high on sensory processing sensitivity (SPS) in response to both positive and negative facial expressions (Acevedo et al, 2014) and to subtle discrepancies in non-social scenic stimuli (Jagiellowicz et al, 2010).…”

Facilitated acquisition of standard but not long delay classical eyeblink conditioning in behaviorally inhibited adolescents

“…Previous research indicates the hippocampus may be involved in risk for anxiety in terms of structure [48], function [49], and behavior [19]. Reduced hippocampal activity in the high AMBI group could enhance learning in standard delay (500-ms) conditioning.…”