Elsevier

NeuroImage

Volume 20, Issue 4, December 2003, Pages 2091-2099
NeuroImage

Regular article
Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage

https://doi.org/10.1016/j.neuroimage.2003.08.006Get rights and content

Abstract

Considerable evidence from both animal and human subject research supports the hypothesis that the amygdala, when activated by emotional arousal, modulates memory storage processes in other brain regions. By this hypothesis, changes in the functional interactions of the amygdala with other brain regions during emotional conditions should underlie, at least in part, enhanced memory for emotional material. Here we examined the influence of the human amygdala on other brain regions under emotional and nonemotional learning conditions using structural equation modeling (SEqM). Eleven male subjects received two PET scans for regional cerebral glucose metabolism—one scan while viewing a series of emotionally provocative (negative) film clips and a second scan while viewing a series of more emotionally neutral film clips. Enhanced activity in the right amygdala was related to enhanced memory for the emotional films. To identify potential candidate voxels for SEqM, the functional connectivity of the maximally activated voxel within the right amygdala was investigated using partial least squares. A subset of regions identified by this analysis showing differences functional connectivity with the amygdala between the emotional versus neutral film conditions were then submitted to SEqM, which revealed significantly increased amygdala influences on the ipsilateral parahippocampal gyrus and ventrolateral prefrontal cortex during the emotional relative to the neutral film viewing condition. These findings support the view that increased influences from the amygdala, presumably reflecting its memory-modulation function, occur during emotionally arousing learning situations.

Section snippets

Experimental procedures

Data for the present study were taken from Cahill et al. (2001). Details of the experimental design are given in this study and in Cahill et al. (1996). Briefly, 11 healthy, right-handed males (average age = 21.5 ± 0.88 years) underwent two PET scans while watching a series of film clips. Exclusionary criteria included any major medical or psychiatric illness, substance abuse, or history of head injury. The PET sessions were separated by 2–7 days. During one scan, subjects viewed 12 emotionally

Behavioral results

Subjects recalled an average of 2.1 (± 0.6) neutral films and 5.73 (± 0.8) emotional films. The average arousal rating for the neutral film clips was 2.8 (± 0.5) and for the emotional film clips was 5.2 (± 0.5). Subjects recalled significantly more emotional films than neutral films [t(10) = 4.1, P < .002] and rated the emotional films as significantly more arousing than the neutral films [t(10) = 3.2, P < .01].

Functional connectivity of the right amygdala

The first LV produced by the seed-PLS (accounting for 81% of the cross-block

Discussion

This experiment tested the hypothesis that increased efferent influences from the amygdala to other brain regions, and in particular to the parahippocampal region, will occur in emotionally arousing compared with emotionally neutral learning conditions. Consistent with this hypothesis, results from an SEqM analysis of PET data revealed a significantly more positive amygdala influence on two brain regions—the parahippocampal gyrus and Brodmann's area 47—during the emotional relative to the

Acknowledgements

We greatly appreciate the expert and detailed anatomical advice offered by James Fallon in the creation of the neuroanatomical model and our wonderful path analysis consultant Randy McIntosh. Funded by NIMH Grant MH57508 to L.C.

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