Memory for fearful faces across development: specialization of amygdala nuclei and medial temporal lobe structures

Abstract

Enhanced memory for emotional faces is a significant component of adaptive social interactions, but little is known on its neural developmental correlates. We explored the role of amygdaloid complex (AC) and medial temporal lobe (MTL) in emotional memory recognition across development, by comparing fMRI activations of successful memory encoding of fearful and neutral faces in children (n = 12; 8–12 years) and adolescents (n = 12; 13–17 years). Memory for fearful faces was enhanced compared with neutral ones in adolescents, as opposed to children. In adolescents, activations associated with successful encoding of fearful faces were centered on baso-lateral AC nuclei, hippocampus, enthorhinal and parahippocampal cortices. In children, successful encoding of fearful faces relied on activations of centro-mesial AC nuclei, which was not accompanied by functional activation of MTL memory structures. Successful encoding of neutral faces depended on activations in anterior MTL region (hippocampal head and body) in adolescents, but more posterior ones (hippocampal tail and parahippocampal cortex) in children. In conclusion, two distinct functional specializations emerge from childhood to adolescence and result in the enhancement of memory for these particular stimuli: the specialization of baso-lateral AC nuclei, which is associated with the expertise in processing emotional facial expression, and which is intimately related to the specialization of MTL memory network. How the interplay between specialization of AC nuclei and of MTL memory structures is fundamental for the edification of social interactions remains to be elucidated.

Intelligibility of Emotional Speech in Younger and Older Adults

“…Furthermore, recent findings suggest that the specialized role of the amygdala in modulating responses to visual emotional information develops during adolescence (Pinabiaux et al 2013), and threat detection, as measured by the speed with which threatening faces are detected in complex visual arrays, does not appear to change with adult aging (Mather & Carstensen 2005;Mather & Knight 2005). This finding extends similar prior findings in the visual domain and suggests that there is a modality-general response to fear that affects multiple aspects of cognitive performance, including speech understanding.…”

Medial prefrontal activity at encoding determines enhanced recognition of threatening faces after 1.5 years

“…Only a few previous studies investigated effects of facial expression on long-term face recognition memory using shorter retention intervals ranging from days to weeks (e.g., Anderson et al, 2006;Gupta and Srinivasan, 2009;Wang, 2013). The present study for the first time demonstrated that recognition memory for faces with threatening emotional expressions was preserved for an extensive period of time of at least 1.5 years, consistent with findings of immediate face recognition (Grady et al, 2007;Keightley et al, 2011;Pinabiaux et al, 2013) and recognition after a 24-h delay (Wang, 2013). This finding is moreover in line with studies showing a memory advantage of negative non-facial stimuli after a retention interval of 1 year (Dolcos et al, 2005;Erk et al, 2010;Gavazzeni et al, 2012).…”

“…These findings broadly align with numerous previous studies that demonstrated a robust emotional enhancement of memory for nonfacial stimuli indicating that emotional events, particularly high-arousing negative ones, are more vividly and accurately remembered over retention intervals ranging from minutes to years (reviewed in Bowen et al, 2018;Yonelinas and Ritchey, 2015). In contrast, examination of specific effects of emotional facial expressions on subsequent recognition revealed inconclusive results and findings varied according to retention intervals (e.g., Anderson et al, 2006;Gupta and Srinivasan, 2009;Mather and Carstensen, 2003;Pinabiaux et al, 2013;Wang, 2013).…”

Atypical Functional Connectivity of Amygdala Related to Reduced Symptom Severity in Children With Autism

“…70 It has been proposed that these connections support associative processing and perception of salience of the sensory input by the amygdala. 71, 72 Indeed, the left inferior occipital cluster showing weaker amygdala connectivity overlapped with the region of the extended face network involved in emotional face encoding, 73 as well as gaze processing. 74 Thus, reduced amygdala-IOG functional connectivity observed here in children and adolescents with ASDs may reflect history of disrupted coordination between amygdala and the regions involved in processing of facial expressions and cues.…”