Striatal Functional Alteration in Adolescents Characterized by Early Childhood Behavioral Inhibition

Abstract

The temperamental style of behavioral inhibition has been characterized by exaggerated behavioral and neural responses to cues signaling threat. Virtually no work, however, has addressed whether behavioral inhibition may also confer heightened brain activation in response to positively valenced incentives. We used event-related functional MRI (fMRI) and a monetary incentive delay task to examine whether the neural response to incentives is also greater in adolescents characterized as behaviorally inhibited early in life compared with those characterized as non-inhibited. Whereas task performance did not differ between groups, fMRI revealed greater striatal activation to incentives in behaviorally inhibited adolescents than in non-inhibited adolescents. This was regardless of whether the incentive was an anticipated gain or loss. Alteration in neural systems underlying behavior modulated by both negative and positive contingencies may represent a correlate of behavioral inhibition that also underlies vulnerability to various forms of developmental psychopathology.

Separation Anxiety in Children and Adolescents

“…According to significance of the amygdala in the startle reflex, this data indicates a potential role of amygdala-based circuits (and hypothetic significance of the bed nucleus of the striaterminalis) in familial risk for anxiety. This report is consistent with a study of increased stratial function to reward in adolescents with temperamental anxiety (Guyer et al, 2006). The meta-analysis of functional magnetic resonance and positron emission tomography studies of post-traumatic stress disorder, social anxiety disorder, and specific phobia in adults showed that all three disorders displayed hyperactivity in amygdala and insula (Etkin & Wager, 2007).…”

Valence and salience contribute to nucleus accumbens activation

“…The lack of distinction between uncertain-gain and uncertain-loss trials is less consistent with previous findings. Several studies using the MID task (e.g., Bjork et al, 2004;Guyer et al, 2006;Knutson et al, 2001;Knutson et al, 2003; have found greater NAcc activation for uncertain gain than loss (but not all; Juckel et al, 2006). The current paradigm used smaller incentives ($3.00 vs. $5.00), which might be too small to elicit this difference.…”

Behavioral Inhibition and Developmental Risk: A Dual-Processing Perspective

“…For such stimuli, the striatum represents a key subcortical structure that interacts with the PFC to support more automatic modes of processing. Guyer et al (2006) found that adolescents with a history of childhood BI showed greater striatal sensitivity to incentives, relative to adolescents without a history of childhood BI. Perez-Edgar et al (2014) suggested that this enhanced sensitivity specifically occurs in the subset of children with BI who possess a particular dopamine-related genotype.…”

“…This includes motor response patterns, markers of activity in the autonomic nervous system (ie, heart rate and vagal tone; Kagan et al, 1987), cortical activity patterns (Calkins et al, 1996;McManis et al, 2002), and neuroendocrine profiles (ie, cortisol; Kagan et al, 1988;Schmidt et al, 1997). Recent advances in neuroscience have allowed this original amygdala-based model to be expanded to include broader perturbations in a distributed neural circuit, encompassing components of the PFC and striatum (Bar-Haim et al, 2009;Bishop et al, 2004;Guyer et al, 2006;Hardee et al, 2013;Helfinstein et al, 2012). Common across these diverse models is an emphasis on the relations between BI and hypersensitivity in neural circuitry rapidly engaged by automatic modes of processing and a resulting behavioral sensitivity to motivationally salient cues.…”