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Basolateral Amygdala Connectivity With Subgenual Anterior Cingulate Cortex Represents Enhanced Fear-Related Memory

Yuko Hakamata¹, Shinya Mizukami², Shuhei Izawa³

¹Department of Behavioral Medicine, National Institute of Mental Health, National Center of Neurology and Psychiatry, Tokyo, Japan; Department of Health Science, Kitasato University School of Allied Health Sciences, Kanagawa, Japan.

Biological Psychiatry. Cognitive Neuroscience and Neuroimaging

|February 1, 2020

Abstract

Background:

The amygdala can enhance emotional memory encoding as well as anxiogenesis via corticotropin-releasing factor neurons. However, the amygdala's explicit role in emotional encoding remains unclarified in humans. We examined how functional connectivity (FC) of amygdala subnuclei affects emotional encoding, considering its mechanism in which anxiety, attention, and cortisol conceivably participate.

Methods:

A total of 65 healthy humans underwent resting-state functional magnetic resonance imaging scans and saliva collection at 10 points in time over 2 days. FC analysis was performed for basolateral amygdala subnucleus (BLA) and centromedial amygdala subnucleus. We assessed attentional control via an emotional Stroop task and assessed emotional encoding via a facial identification task that examines how strongly a neutral face is memorized when accompanied by an emotional face (fearful, sad, or happy). FC and task performance were compared between high-anxious and non-high-anxious groups classified by anxious personality scores.

Results:

BLA connected with subgenual anterior cingulate cortex (sgACC) in proportion to the strength of fear-related encoding, whereas centromedial subnucleus connected with caudate nucleus for happy-related encoding. The high-anxious group showed more enhanced fear-related encoding but impaired happy-related encoding compared with the non-high-anxious group. BLA-sgACC FC was more intensified in the high-anxious group than in the non-high-anxious group; however, centromedial-caudate FC did not differ between them. Although emotional encoding was uncorrelated with either attentional control or cortisol, BLA-sgACC was positively correlated with cortisol increase after awakening.

Conclusions:

The study revealed that neural interactions of BLA, specifically with sgACC, might play a critical role in fear-related memory encoding, depending on the individual's level of anxiety. These findings aid in understanding the complicated mechanisms of emotional memory in anxiety disorders.

Keywords:

Anxious personality trait Attention Cognitive bias Memory Rostral anterior cingulate cortex Total cortisol output

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