Amygdalar reactivity is associated with prefrontal cortical thickness in a large population-based sample of adolescents

IMAGEN Consortium

doi:10.1371/journal.pone.0216152

Amygdalar reactivity is associated with prefrontal cortical thickness in a large population-based sample of adolescents

IMAGEN Consortium

University of Vermont
McGill University
Universitatsklinikum Mannheim
Department of Urology
Universitatsklinikum Hamburg-Eppendorf und Medizinische Fakultat
MRC Medical Research Council
Heidelberg University
Université Paris-Saclay
University of Nottingham
Institute for Radiology, CCM
Physikalisch-Technische Bundesanstalt
University of Paris XI - University of Paris-Sud
University Health Network, Toronto
University Medical Center Göttingen
TU Dresden

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7 Citations (Scopus)

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Abstract

In structural neuroimaging studies, reduced cerebral cortical thickness in orbital and ventromedial prefrontal regions is frequently interpreted as reflecting an impaired ability to downregulate neuronal activity in the amygdalae. Unfortunately, little research has been conducted in order to test this conjecture. We examine the extent to which amygdalar reactivity is associated with cortical thickness in a population-based sample of adolescents. Data were obtained from the IMAGEN study, which includes 2,223 adolescents. While undergoing functional neuroimaging, participants passively viewed video clips of a face that started from a neutral expression and progressively turned angry, or, instead, turned to a second neutral expression. Left and right amygdala ROIs were used to extract mean BOLD signal change for the angry minus neutral face contrast for all subjects. T1-weighted images were processed through the CIVET pipeline (version 2.1.0). In variable-centered analyses, local cortical thickness was regressed against amygdalar reactivity using first and second-order linear models. In a follow-up person-centered analysis, we defined a “high reactive” group of participants based on mean amygdalar BOLD signal change for the angry minus neutral face contrast. Between-group differences in cortical thickness were examined (“high reactive” versus all other participants). A significant association was revealed between the continuous measure of amygdalar reactivity and bilateral ventromedial prefrontal cortical thickness in a second-order linear model (p < 0.05, corrected). The “high reactive” group, in comparison to all other participants, possessed reduced cortical thickness in bilateral orbital and ventromedial prefrontal cortices, bilateral anterior temporal cortices, left caudal middle temporal gyrus, and the left inferior and middle frontal gyri (p < 0.05, corrected). Results are consistent with non-human primate studies, and provide empirical support for an association between reduced prefrontal cortical thickness and amygdalar reactivity. Future research will likely benefit from investigating the degree to which psychopathology qualifies relations between prefrontal cortical structure and amygdalar reactivity.

Original language	English
Article number	e0216152
Number of pages	16
Journal	PLoS ONE
Volume	14
Issue number	5
DOIs	https://doi.org/10.1371/journal.pone.0216152
Publication status	Published - 2 May 2019

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Amygdalar reactivity_ALBAUGH_Accepted15April2019_GOLD VoRFinal published version, 1.42 MBLicence: CC BY

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@article{b2ba46d57a1a47d398c89bd7dfe3f590,

title = "Amygdalar reactivity is associated with prefrontal cortical thickness in a large population-based sample of adolescents",

abstract = "In structural neuroimaging studies, reduced cerebral cortical thickness in orbital and ventromedial prefrontal regions is frequently interpreted as reflecting an impaired ability to downregulate neuronal activity in the amygdalae. Unfortunately, little research has been conducted in order to test this conjecture. We examine the extent to which amygdalar reactivity is associated with cortical thickness in a population-based sample of adolescents. Data were obtained from the IMAGEN study, which includes 2,223 adolescents. While undergoing functional neuroimaging, participants passively viewed video clips of a face that started from a neutral expression and progressively turned angry, or, instead, turned to a second neutral expression. Left and right amygdala ROIs were used to extract mean BOLD signal change for the angry minus neutral face contrast for all subjects. T1-weighted images were processed through the CIVET pipeline (version 2.1.0). In variable-centered analyses, local cortical thickness was regressed against amygdalar reactivity using first and second-order linear models. In a follow-up person-centered analysis, we defined a “high reactive” group of participants based on mean amygdalar BOLD signal change for the angry minus neutral face contrast. Between-group differences in cortical thickness were examined (“high reactive” versus all other participants). A significant association was revealed between the continuous measure of amygdalar reactivity and bilateral ventromedial prefrontal cortical thickness in a second-order linear model (p < 0.05, corrected). The “high reactive” group, in comparison to all other participants, possessed reduced cortical thickness in bilateral orbital and ventromedial prefrontal cortices, bilateral anterior temporal cortices, left caudal middle temporal gyrus, and the left inferior and middle frontal gyri (p < 0.05, corrected). Results are consistent with non-human primate studies, and provide empirical support for an association between reduced prefrontal cortical thickness and amygdalar reactivity. Future research will likely benefit from investigating the degree to which psychopathology qualifies relations between prefrontal cortical structure and amygdalar reactivity.",

author = "Albaugh, \{Matthew D.\} and Hudziak, \{James J.\} and Catherine Orr and Spechler, \{Philip A.\} and Bader Chaarani and Scott Mackey and Claude Lepage and Vladimir Fonov and Pierre Rioux and Evans, \{Alan C.\} and Tobias Banaschewski and Bokde, \{Arun L.W.\} and Uli Bromberg and Christian B{\"u}chel and Quinlan, \{Erin Burke\} and Sylvane Desrivi{\`e}res and Herta Flor and Antoine Grigis and Penny Gowland and Andreas Heinz and Bernd Ittermann and Martinot, \{Jean Luc\} and Martinot, \{Marie Laure Paill{\`e}re\} and Frauke Nees and Orfanos, \{Dimitri Papadopoulos\} and Tom{\'a}{\v s} Paus and Luise Poustka and Sabina Millenet and Fr{\"o}hner, \{Juliane H.\} and Smolka, \{Michael N.\} and Henrik Walter and Robert Whelan and Gunter Schumann and Potter, \{Alexandra S.\} and Hugh Garavan and \{IMAGEN Consortium\}",

year = "2019",

month = may,

day = "2",

doi = "10.1371/journal.pone.0216152",

language = "English",

volume = "14",

journal = "PLoS ONE",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "5",

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TY - JOUR

T1 - Amygdalar reactivity is associated with prefrontal cortical thickness in a large population-based sample of adolescents

AU - Albaugh, Matthew D.

AU - Hudziak, James J.

AU - Orr, Catherine

AU - Spechler, Philip A.

AU - Chaarani, Bader

AU - Mackey, Scott

AU - Lepage, Claude

AU - Fonov, Vladimir

AU - Rioux, Pierre

AU - Evans, Alan C.

AU - Banaschewski, Tobias

AU - Bokde, Arun L.W.

AU - Bromberg, Uli

AU - Büchel, Christian

AU - Quinlan, Erin Burke

AU - Desrivières, Sylvane

AU - Flor, Herta

AU - Grigis, Antoine

AU - Gowland, Penny

AU - Heinz, Andreas

AU - Ittermann, Bernd

AU - Martinot, Jean Luc

AU - Martinot, Marie Laure Paillère

AU - Nees, Frauke

AU - Orfanos, Dimitri Papadopoulos

AU - Paus, Tomáš

AU - Poustka, Luise

AU - Millenet, Sabina

AU - Fröhner, Juliane H.

AU - Smolka, Michael N.

AU - Walter, Henrik

AU - Whelan, Robert

AU - Schumann, Gunter

AU - Potter, Alexandra S.

AU - Garavan, Hugh

AU - IMAGEN Consortium

PY - 2019/5/2

Y1 - 2019/5/2

N2 - In structural neuroimaging studies, reduced cerebral cortical thickness in orbital and ventromedial prefrontal regions is frequently interpreted as reflecting an impaired ability to downregulate neuronal activity in the amygdalae. Unfortunately, little research has been conducted in order to test this conjecture. We examine the extent to which amygdalar reactivity is associated with cortical thickness in a population-based sample of adolescents. Data were obtained from the IMAGEN study, which includes 2,223 adolescents. While undergoing functional neuroimaging, participants passively viewed video clips of a face that started from a neutral expression and progressively turned angry, or, instead, turned to a second neutral expression. Left and right amygdala ROIs were used to extract mean BOLD signal change for the angry minus neutral face contrast for all subjects. T1-weighted images were processed through the CIVET pipeline (version 2.1.0). In variable-centered analyses, local cortical thickness was regressed against amygdalar reactivity using first and second-order linear models. In a follow-up person-centered analysis, we defined a “high reactive” group of participants based on mean amygdalar BOLD signal change for the angry minus neutral face contrast. Between-group differences in cortical thickness were examined (“high reactive” versus all other participants). A significant association was revealed between the continuous measure of amygdalar reactivity and bilateral ventromedial prefrontal cortical thickness in a second-order linear model (p < 0.05, corrected). The “high reactive” group, in comparison to all other participants, possessed reduced cortical thickness in bilateral orbital and ventromedial prefrontal cortices, bilateral anterior temporal cortices, left caudal middle temporal gyrus, and the left inferior and middle frontal gyri (p < 0.05, corrected). Results are consistent with non-human primate studies, and provide empirical support for an association between reduced prefrontal cortical thickness and amygdalar reactivity. Future research will likely benefit from investigating the degree to which psychopathology qualifies relations between prefrontal cortical structure and amygdalar reactivity.

AB - In structural neuroimaging studies, reduced cerebral cortical thickness in orbital and ventromedial prefrontal regions is frequently interpreted as reflecting an impaired ability to downregulate neuronal activity in the amygdalae. Unfortunately, little research has been conducted in order to test this conjecture. We examine the extent to which amygdalar reactivity is associated with cortical thickness in a population-based sample of adolescents. Data were obtained from the IMAGEN study, which includes 2,223 adolescents. While undergoing functional neuroimaging, participants passively viewed video clips of a face that started from a neutral expression and progressively turned angry, or, instead, turned to a second neutral expression. Left and right amygdala ROIs were used to extract mean BOLD signal change for the angry minus neutral face contrast for all subjects. T1-weighted images were processed through the CIVET pipeline (version 2.1.0). In variable-centered analyses, local cortical thickness was regressed against amygdalar reactivity using first and second-order linear models. In a follow-up person-centered analysis, we defined a “high reactive” group of participants based on mean amygdalar BOLD signal change for the angry minus neutral face contrast. Between-group differences in cortical thickness were examined (“high reactive” versus all other participants). A significant association was revealed between the continuous measure of amygdalar reactivity and bilateral ventromedial prefrontal cortical thickness in a second-order linear model (p < 0.05, corrected). The “high reactive” group, in comparison to all other participants, possessed reduced cortical thickness in bilateral orbital and ventromedial prefrontal cortices, bilateral anterior temporal cortices, left caudal middle temporal gyrus, and the left inferior and middle frontal gyri (p < 0.05, corrected). Results are consistent with non-human primate studies, and provide empirical support for an association between reduced prefrontal cortical thickness and amygdalar reactivity. Future research will likely benefit from investigating the degree to which psychopathology qualifies relations between prefrontal cortical structure and amygdalar reactivity.

UR - https://www.scopus.com/pages/publications/85065588405

U2 - 10.1371/journal.pone.0216152

DO - 10.1371/journal.pone.0216152

M3 - Article

C2 - 31048888

AN - SCOPUS:85065588405

SN - 1932-6203

VL - 14

JO - PLoS ONE

JF - PLoS ONE

IS - 5

M1 - e0216152

ER -

Amygdalar reactivity is associated with prefrontal cortical thickness in a large population-based sample of adolescents

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