Translation of monosynaptic circuits underlying amygdala fMRI neurofeedback training.


Journal

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907

Informations de publication

Date de publication:
05 Aug 2024
Historique:
received: 04 06 2024
accepted: 23 07 2024
revised: 16 07 2024
medline: 6 8 2024
pubmed: 6 8 2024
entrez: 5 8 2024
Statut: aheadofprint

Résumé

fMRI neurofeedback using autobiographical memory recall to upregulate the amygdala is associated with resting-state functional connectivity (rsFC) changes between the amygdala and the salience and default mode networks (SN and DMN, respectively). We hypothesize the existence of anatomical circuits underlying these rsFC changes. Using a cross-species brain parcellation, we identified in non-human primates locations homologous to the regions of interest (ROIs) from studies showing pre-to-post-neurofeedback changes in rsFC with the left amygdala. We injected bidirectional tracers in the basolateral, lateral, and central amygdala nuclei of adult macaques and used bright- and dark-field microscopy to identify cells and axon terminals in each ROI (SN: anterior cingulate, ventrolateral, and insular cortices; DMN: temporal pole, middle frontal gyrus, angular gyrus, precuneus, posterior cingulate cortex, parahippocampal gyrus, hippocampus, and thalamus). We also performed additional injections in specific ROIs to validate the results following amygdala injections and delineate potential disynaptic pathways. Finally, we used high-resolution diffusion MRI data from four post-mortem macaque brains and one in vivo human brain to translate our findings to the neuroimaging domain. Different amygdala nuclei had significant monosynaptic connections with all the SN and DMN ipsilateral ROIs. Amygdala connections with the DMN contralateral ROIs are disynaptic through the hippocampus and parahippocampal gyrus. Diffusion MRI in both species benefitted from using the ground-truth tracer data to validate its findings, as we identified false-negative ipsilateral and false-positive contralateral connectivity results. This study provides the foundation for future causal investigations of amygdala neurofeedback modulation of the SN and DMN through these anatomic connections.

Identifiants

pubmed: 39103495
doi: 10.1038/s41386-024-01944-w
pii: 10.1038/s41386-024-01944-w
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : K99-MH130648
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : P50-MH106435
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : R01-MH045573
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Biomedical Imaging and Bioengineering (NIBIB)
ID : R01-EB021265
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Biomedical Imaging and Bioengineering (NIBIB)
ID : R01-EB021265
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Biomedical Imaging and Bioengineering (NIBIB)
ID : R01-EB021265
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R01-NS119911
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R01-NS119911
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R01-NS119911

Informations de copyright

© 2024. The Author(s).

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Auteurs

Lucas Trambaiolli (L)

McLean Hospital, Harvard Medical School, Boston, MA, USA. ltrambaiolli@mclean.harvard.edu.
Department of Pharmacology and Physiology, University of Rochester, Rochester, NY, USA. ltrambaiolli@mclean.harvard.edu.

Chiara Maffei (C)

Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA.

Evan Dann (E)

Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.

Claudinei Biazoli (C)

Center for Mathematics Computation and Cognition, Federal University of ABC, Santo André, Brazil.
School of Biological and Behavioural Sciences, Queen Mary University of London, London, UK.

Gleb Bezgin (G)

Neuroinformatics for Personalized Medicine lab, Montreal Neurological Institute, McGill University, Montréal, QC, Canada.

Anastasia Yendiki (A)

Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.

Suzanne Haber (S)

McLean Hospital, Harvard Medical School, Boston, MA, USA. suzanne_haber@urmc.rochester.edu.
Department of Pharmacology and Physiology, University of Rochester, Rochester, NY, USA. suzanne_haber@urmc.rochester.edu.

Classifications MeSH