Alterations in amygdala functional connectivity reflect early temperament

Abstract

Behavioral inhibition (BI) is a temperament identified early in life that is associated with increased risk for anxiety disorders. Amygdala hyperresponsivity, found both in behaviorally inhibited and anxious individuals, suggests that amygdala dysfunction may represent a marker of anxiety risk. However, broader amygdala networks have not been examined in individuals with a history of childhood BI. This study uses resting state fMRI to assess amygdala intrinsic functional connectivity (iFC) in 38 healthy young adults (19 with a history of BI, 19 with no history of BI) selected from a longitudinal study. Centromedial, basolateral, and superficial amygdala iFCs were compared between groups and examined in relation to self-report measures of anxiety. Group differences were observed in amygdala iFC with prefrontal cortex, striatum, anterior insula, and cerebellum. Adults characterized with BI in childhood endorsed greater state anxiety prior to entering the scanner, which was associated with several of the group differences. Findings support enduring effects of BI on amygdala circuitry, even in the absence of current psychopathology.

Shyness and Trajectories of Functional Network Connectivity Over Early Adolescence

“…Previous authors have described selective increases in DMN rs‐fc as reflecting an “internal shift” that may be a feature of highly shy individuals (Taber‐Thomas et al., ). In contrast to the current results, other studies have reported shyness‐related variation in functional connectivity (Roy et al., ; Taber‐Thomas et al., ), task‐related activity (Clauss et al., ; Guyer et al., , ), and structure (Schwartz et al., ; Sylvester et al., ) in networks beyond the DMN. The most likely explanation for this discrepancy is the specific developmental period of subjects in the different studies.…”

“…Additional consistently described brain differences in children with high versus low shyness include increased activity in the amygdala to emotionally evocative faces (Pérez‐Edgar et al., ; Schwartz, Wright, Shin, Kagan, & Rauch, ); alterations in activity in the nucleus accumbens, striatum, and other subcortical areas during reward processing (Guyer et al., , ); and structural and functional alterations in brain regions involved in directing attention and cognitive control, such as the FPN, SN, and VAN networks described earlier (Guyer et al., ; Jarcho, Fox, Pine, Etkin, et al., ; Jarcho, Fox, Pine, Leibenluft, et al., ; Sylvester et al., ). Cross‐sectional studies using rs‐fc have indicated that shyness or behavioral inhibition is associated with variation of connectivity of the amygdala as well as regions within the DMN, SN, FPN, VAN, and somatosensory networks (Clauss, Benningfield, Rao, & Blackford, ; Rogers et al., ; Roy et al., ; Sylvester et al., ; Taber‐Thomas, Morales, Hillary, & Pérez‐Edgar, ). Together, these cross‐sectional data suggest that shyness is marked by alterations in connectivity both in brain systems involved in self‐directed processing (e.g., the DMN) and externally focused processing (e.g., the FPN).…”

Developmental sex differences in resting state functional connectivity of amygdala sub-regions

“…The SFA is the most conserved amygdala sub-region and it is thought to play an important role in social communication via olfactory (Bzdok et al, 2013a) and social cues (Goossens et al, 2009, Bzdok et al, 2013a); therefore, increasing RSFC between this sub-region and the parieto-occipital cortex could indicate that adolescent girls have relatively compromised socio-emotional processing. This interpretation is supported by studies conducted in adults showing functional connectivity of parieto-occipital cortex with SFA is linked with childhood behavioral inhibition (Roy et al, 2014) and current social inhibition (Blackford et al, 2014). A different study showed that administration of allopregnanolone reduced connectivity between the amygdala and parietal cortex, which was also correlated with reductions in negative affect (Sripada et al, 2014).…”

Frontolimbic functioning during threat-related attention: Relations to early behavioral inhibition and anxiety in children

“…Anxious adolescents display a hyperactive amygdala response to brief (17ms) face presentation times, marking an initial pre-conscious response to threat presentation, that may be dampened when regulatory mechanisms can be invoked at longer (500ms) stimulus presentation times (Monk et al, 2006; 2008). Adults with a history of BI show more negative amygdala-dlPFC connectivity both during responses to threat-versus-angry faces (Hardee et al, 2013) and in resting state (Roy et al, 2014), suggesting that atypical dynamics in this circuitry might be a marker of temperamental risk for anxiety. Future research is needed to compare the magnitude and directionality of amygdala-dlPFC functional connectivity between behaviorally inhibited and non-inhibited children.…”