Contributions of Human Amygdala Nuclei to Resting-state Networks

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2022 Dec 28

PMID 36576924

Authors

Uriel K A Elvira

Sara Seoane

Joost Janssen

Niels Janssen

Affiliations

Soon will be listed here.

Abstract

The amygdala is a brain region with a complex internal structure that is associated with psychiatric disease. Methodological limitations have complicated the study of the internal structure of the amygdala in humans. In the current study we examined the functional connectivity between nine amygdaloid nuclei and existing resting-state networks using a high spatial-resolution fMRI dataset. Using data-driven analysis techniques we found that there were three main clusters inside the amygdala that correlated with the somatomotor, ventral attention and default mode networks. In addition, we found that each resting-state networks depended on a specific configuration of amygdaloid nuclei. Finally, we found that co-activity in the cortical-nucleus increased with the severity of self-rated fear in participants. These results highlight the complex nature of amygdaloid connectivity that is not confined to traditional large-scale divisions, implicates specific configurations of nuclei with certain resting-state networks and highlights the potential clinical relevance of the cortical-nucleus in future studies of the human amygdala.

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References

Kong Y, Eippert F, Beckmann C, Andersson J, Finsterbusch J, Buchel C . Intrinsically organized resting state networks in the human spinal cord. Proc Natl Acad Sci U S A. 2014; 111(50):18067-72. PMC: 4273395. DOI: 10.1073/pnas.1414293111. View

He X, Chaitanya G, Asma B, Caciagli L, Bassett D, Tracy J . Disrupted basal ganglia-thalamocortical loops in focal to bilateral tonic-clonic seizures. Brain. 2019; 143(1):175-190. PMC: 7954388. DOI: 10.1093/brain/awz361. View

Ganella D, Kim J . Developmental rodent models of fear and anxiety: from neurobiology to pharmacology. Br J Pharmacol. 2014; 171(20):4556-74. PMC: 4209932. DOI: 10.1111/bph.12643. View

Glasser M, Sotiropoulos S, Wilson J, Coalson T, Fischl B, Andersson J . The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage. 2013; 80:105-24. PMC: 3720813. DOI: 10.1016/j.neuroimage.2013.04.127. View

Dale A, Fischl B, Sereno M . Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999; 9(2):179-94. DOI: 10.1006/nimg.1998.0395. View

Zhang L, Hu X, Lu L, Li B, Hu X, Bu X . Anatomic alterations across amygdala subnuclei in medication-free patients with obsessive-compulsive disorder. J Psychiatry Neurosci. 2020; 45(5):334-343. PMC: 7850150. DOI: 10.1503/jpn.190114. View

Alsady T, Blessing E, Beissner F . MICA-A toolbox for masked independent component analysis of fMRI data. Hum Brain Mapp. 2016; 37(10):3544-56. PMC: 6867364. DOI: 10.1002/hbm.23258. View

Nogovitsyn N, Souza R, Muller M, Srajer A, Metzak P, Hassel S . Aberrant limbic brain structures in young individuals at risk for mental illness. Psychiatry Clin Neurosci. 2020; 74(5):294-302. DOI: 10.1111/pcn.12985. View

Ousdal O, Specht K, Server A, Andreassen O, Dolan R, Jensen J . The human amygdala encodes value and space during decision making. Neuroimage. 2014; 101:712-9. PMC: 4176653. DOI: 10.1016/j.neuroimage.2014.07.055. View

10.

Brown S, Rutland J, Verma G, Feldman R, Alper J, Schneider M . Structural MRI at 7T reveals amygdala nuclei and hippocampal subfield volumetric association with Major Depressive Disorder symptom severity. Sci Rep. 2019; 9(1):10166. PMC: 6629636. DOI: 10.1038/s41598-019-46687-7. View

11.

Ezama L, Hernandez-Cabrera J, Seoane S, Pereda E, Janssen N . Functional connectivity of the hippocampus and its subfields in resting-state networks. Eur J Neurosci. 2021; 53(10):3378-3393. PMC: 8252772. DOI: 10.1111/ejn.15213. View

12.

Balleine B, Killcross S . Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci. 2006; 29(5):272-9. DOI: 10.1016/j.tins.2006.03.002. View

13.

Peck C, Lau B, Salzman C . The primate amygdala combines information about space and value. Nat Neurosci. 2013; 16(3):340-8. PMC: 3596258. DOI: 10.1038/nn.3328. View

14.

Roy A, Shehzad Z, Margulies D, Kelly A, Uddin L, Gotimer K . Functional connectivity of the human amygdala using resting state fMRI. Neuroimage. 2008; 45(2):614-26. PMC: 2735022. DOI: 10.1016/j.neuroimage.2008.11.030. View

15.

Adolphs R . What does the amygdala contribute to social cognition?. Ann N Y Acad Sci. 2010; 1191:42-61. PMC: 2871162. DOI: 10.1111/j.1749-6632.2010.05445.x. View

16.

McDonald A, Mascagni F . Projections of the lateral entorhinal cortex to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience. 1997; 77(2):445-59. DOI: 10.1016/s0306-4522(96)00478-2. View

17.

Likhtik E, Stujenske J, Topiwala M, Harris A, Gordon J . Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nat Neurosci. 2013; 17(1):106-13. PMC: 4035371. DOI: 10.1038/nn.3582. View

18.

Sylvester C, Yu Q, Srivastava A, Marek S, Zheng A, Alexopoulos D . Individual-specific functional connectivity of the amygdala: A substrate for precision psychiatry. Proc Natl Acad Sci U S A. 2020; 117(7):3808-3818. PMC: 7035483. DOI: 10.1073/pnas.1910842117. View

19.

Bzdok D, Laird A, Zilles K, Fox P, Eickhoff S . An investigation of the structural, connectional, and functional subspecialization in the human amygdala. Hum Brain Mapp. 2012; 34(12):3247-66. PMC: 4801486. DOI: 10.1002/hbm.22138. View

20.

Raber J, Arzy S, Bertolus J, Depue B, Haas H, Hofmann S . Current understanding of fear learning and memory in humans and animal models and the value of a linguistic approach for analyzing fear learning and memory in humans. Neurosci Biobehav Rev. 2019; 105:136-177. DOI: 10.1016/j.neubiorev.2019.03.015. View