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Connectivity between the central nucleus of the amygdala and the bed nucleus of the stria terminalis in the non-human primate: neuronal tract tracing and developmental neuroimaging studies

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Abstract

The lateral division of the bed nucleus of the stria terminalis (BSTL) and central nucleus of the amygdala (Ce) form the two poles of the ‘central extended amygdala’, a theorized subcortical macrostructure important in threat-related processing. Our previous work in nonhuman primates, and humans, demonstrating strong resting fMRI connectivity between the Ce and BSTL regions, provides evidence for the integrated activity of these structures. To further understand the anatomical substrates that underlie this coordinated function, and to investigate the integrity of the central extended amygdala early in life, we examined the intrinsic connectivity between the Ce and BSTL in non-human primates using ex vivo neuronal tract tracing, and in vivo diffusion-weighted imaging and resting fMRI techniques. The tracing studies revealed that BSTL receives strong input from Ce; however, the reciprocal pathway is less robust, implying that the primate Ce is a major modulator of BSTL function. The sublenticular extended amygdala (SLEAc) is strongly and reciprocally connected to both Ce and BSTL, potentially allowing the SLEAc to modulate information flow between the two structures. Longitudinal early-life structural imaging in a separate cohort of monkeys revealed that extended amygdala white matter pathways are in place as early as 3 weeks of age. Interestingly, resting functional connectivity between Ce and BSTL regions increases in coherence from 3 to 7 weeks of age. Taken together, these findings demonstrate a time period during which information flow between Ce and BSTL undergoes postnatal developmental changes likely via direct Ce → BSTL and/or Ce ↔ SLEAc ↔ BSTL projections.

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Abbreviations

Ac:

Anterior commissure

ABmc:

Accessory basal nucleus, magnocellular subdivision

Astr:

Amygdalostriatal transition zone

Bi:

Basal nucleus, intermediate subdivision

Bmc:

Basal nucleus, magnocellular subdivision

Bpc:

Basal nucleus, parvicellular subdivision

BST:

Bed nucleus of the stria terminalis

BSTL:

Lateral bed nucleus of the stria terminalis

BSTLc:

Lateral bed nucleus of the stria terminalis, capsular subdivision

BSTLcn:

Lateral bed nucleus of the stria terminalis, central subdivision

BSTLj:

Lateral bed nucleus of the stria terminalis, juxtacapsular subdivision

BSTLP:

Lateral bed nucleus of the stria terminalis, posterior subdivision

C:

Caudate nucleus

Ce:

Central nucleus

CeLcn:

Central nucleus, lateral central subdivision

CeLc:

Central nucleus, lateral capsular subdivision

CeM:

Central nucleus, medial subdivision

EAc:

Central extended amygdala

GP:

Globus pallidus

GPe:

Globus pallidus, pars externa

GPi:

Globus pallidus, pars interna

H:

Hippocampus

Ic:

Internal capsule

L:

Lateral nucleus

M:

Medial nucleus

NBM:

Nucleus basalis of Meynert

P:

Putamen

S:

Shell of the ventral striatum

SLEAc:

Sublenticular extended amygdala, central subdivision

ST:

Stria terminalis

V:

Ventricle

VA:

Ventral amygdalofugal pathway

VP:

Ventral pallidum

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Acknowledgments

We gratefully acknowledge the technical expertise of Ms. Nanette Alcock and thank the personnel of the Harlow Center for Biological Psychology, the HealthEmotions Research Institute, the Waisman Laboratory for Brain Imaging and Behavior, and the Wisconsin National Primate Research Center (WNPRC). This research was conducted in part at a facility constructed with support from Research Facilities Improvement Program Grant numbers RR15459-01 and RR020141-01. This work was supported by Grants from the National Institutes of Health: P51OD011106 (WNPRC); R01-MH063291 (JLF); F30-MH096502 (DMD); R01-MH046729 (NHK); R01-MH081884 (NHK); P50-MH100031 (RJD, NHK); T32 NS007-489-09 (LMC) and T32-MH018931-25. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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    Authors and Affiliations

    1. Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, Madison, USA

      Jonathan A. Oler, Do P. M. Tromp, Andrew S. Fox, Rothem Kovner, Richard J. Davidson, Andrew L. Alexander, Daniel R. McFarlin, Rasmus M. Birn & Ned H. Kalin

    2. Department of Psychology, University of Wisconsin-Madison, Madison, USA

      Andrew S. Fox, Richard J. Davidson & Ned H. Kalin

    3. Department of Medical Physics, University of Wisconsin School of Medicine and Public Health, Madison, USA

      Andrew L. Alexander & Rasmus M. Birn

    4. Allegheny College, Meadville, USA

      Benjamin E. Berg

    5. Department of Neuroscience, University of Rochester Medical Center, Rochester, USA

      Danielle M. deCampo & Julie L. Fudge

    6. Department of Psychiatry, University of Rochester Medical Center, Rochester, USA

      Julie L. Fudge

    7. HealthEmotions Research Institute, Wisconsin Psychiatric Institute and Clinics, 6001 Research Park Blvd., Madison, WI, 53719, USA

      Jonathan A. Oler, Do P. M. Tromp, Andrew S. Fox, Rothem Kovner, Daniel R. McFarlin & Ned H. Kalin

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    Conflict of interest

    Dr. Kalin has received honoraria from CME Outfitters, Elsevier, and the Pritzker Neuropsychiatric Disorders Research Consortium. He is on the Advisory Boards for Corcept Therapeutics and Skyland Trail-George West Mental Health Foundation. Dr. Kalin is a Stockholder in Corcept Therapeutics, and owns several patents including: promoter sequences for corticotropin-releasing factor alpha (U.S. Patent #7071323, issued on 07-04-06); a method of identifying agents that alter the activity of the promoter sequences (U.S. Patent #7531356 issued on 05-12-09); promoter sequences for urocortin II and the use thereof (U.S. Patent #7087385 issued on 08-08-06); and promoter sequences for corticotropin-releasing factor binding protein and use thereof (U.S. Patent #7122650, issued on 10-17-06). All other authors declare no conflicts of interest.

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    J. A. Oler and D. P. M. Tromp contributed equally to this manuscript.

    J. L. Fudge and N. H. Kalin share senior authorship.

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    Oler, J.A., Tromp, D.P.M., Fox, A.S. et al. Connectivity between the central nucleus of the amygdala and the bed nucleus of the stria terminalis in the non-human primate: neuronal tract tracing and developmental neuroimaging studies. Brain Struct Funct 222, 21–39 (2017). https://doi.org/10.1007/s00429-016-1198-9

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