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Structure related to function: prefrontal surface area has an indirect effect on the relationship between amygdala volume and trait neuroticism

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Abstract

Trait neuroticism refers to individual differences in negative emotional response to threat, frustration, or loss, operationally defined by elevated levels of irritability, anger, sadness, anxiety, worry, hostility, self-consciousness, and vulnerability to mental and physical difficulties. While functional studies have been fairly consistent when identifying regions associated with neuroticism during emotional stimuli, structural imagining studies do not tend to find a relationship between amygdala volume and trait neuroticism. There is a great deal of functional evidence that frontoparietal areas are related to the amygdala, and to emotional reactivity more generally, as a function of their involvement in emotion regulation. Specifically, top–down emotion appraisal and expression appear to involve parts of the dorsolateral and dorsomedial prefrontal cortices, which operate at least in part via the indirect modulation of the amygdala. It was hypothesized that cortical surface area and cortical thickness in regions associated with emotion appraisal/expression and emotional attention (i.e., superior frontal and rostral middle frontal gyri, respectively) would have an indirect effect on the relationship between amygdala volume and self-reported neuroticism (respectively), potentially explaining the inconsistency in the structural literature. In sample of 1106 adults, superior frontal and rostral middle frontal gyri, as parcellated by Freesurfer, were examined as potentially restricting variance in a model of indirect effects, which may elucidate the overall relationship between cortical and subcortical gray matter volume and trait neuroticism. Results indicated that, despite no association between bilateral amygdala volume and trait neuroticism, when right superior frontal surface area was entered into the model of indirect effects, a significant relationship between amygdala volume and trait neuroticism emerged. Two of the three remaining models indicated that cortical surface area had an indirect effect on the relationship between amygdala volume and trait neuroticism. These findings highlight the relationship between structural and functional neuroimaging studies. Specifically, the results indicate that when volume is related to behavior, individual differences in higher-order cortical regions, particularly surface area, may help to better understand the relationship between emotion and subcortical gray matter volume.

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Acknowledgements

Data were provided [in part] by the Human Connectome Project, WU-Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research; and by the McDonnell Center for Systems Neuroscience at Washington University.

Funding

Data were provided [in part] by the Human Connectome Project, WU-Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research; and by the McDonnell Center for Systems Neuroscience at Washington University. A small internal grant from Louisiana State University (i.e., Strategic Research Grant) aided in allowing for computer hardware to make storage of the data possible.

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    Peter J. Castagna

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Castagna, P.J. Structure related to function: prefrontal surface area has an indirect effect on the relationship between amygdala volume and trait neuroticism. Brain Struct Funct 224, 3309–3320 (2019). https://doi.org/10.1007/s00429-019-01974-x

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