Brain Structure and Function

, Volume 223, Issue 6, pp 2685–2698 | Cite as

Paraventricular hypothalamic and amygdalar CRF neurons synapse in the external globus pallidus

  • Albert J. HuntJr.
  • Rajan Dasgupta
  • Shivakumar Rajamanickam
  • Zhiying Jiang
  • Michael Beierlein
  • C. Savio Chan
  • Nicholas J. Justice
Original Article


Stress evokes directed movement to escape or hide from potential danger. Corticotropin-releasing factor (CRF) neurons are highly activated by stress; however, it remains unclear how this activity participates in stress-evoked movement. The external globus pallidus (GPe) expresses high levels of the primary receptor for CRF, CRFR1, suggesting the GPe may serve as an entry point for stress-relevant information to reach basal ganglia circuits, which ultimately gate motor output. Indeed, projections from CRF neurons are present within the GPe, making direct contact with CRFR1-positive neurons. CRFR1 expression is heterogenous in the GPe; prototypic GPe neurons selectively express CRFR1, while arkypallidal neurons do not. Moreover, CRFR1-positive GPe neurons are excited by CRF via activation of CRFR1, while nearby CRFR1-negative neurons do not respond to CRF. Using monosynaptic rabies viral tracing techniques, we show that CRF neurons in the stress-activated paraventricular nucleus of the hypothalamus (PVN), central nucleus of the amygdala (CeA), and bed nucleus of the stria terminalis (BST) make synaptic connections with CRFR1-positive neurons in the GPe an unprecedented circuit connecting the limbic system with the basal ganglia. CRF neurons also make synapses on Npas1 neurons, although the majority of Npas1 neurons are arkypallidal and do not express CRFR1. Interestingly, prototypic and arkypallidal neurons receive different patterns of innervation from CRF-rich nuclei. Hypothalamic CRF neurons preferentially target prototypic neurons, while amygdalar CRF neurons preferentially target arkypallidal neurons, suggesting that these two inputs to the GPe may have different impacts on GPe output. Together, these data describe a novel neural circuit by which stress-relevant information carried by the limbic system signals in the GPe via CRF to influence motor output.


CRF CRH CRFR1 CRHR1 Globus pallidus Stress 



The authors thank Z. Mao who provided expertise in confocal microscopy. We thank L. Mangieri and Q. Tong for their valuable input to data interpretation and resource sharing. We thank J. Selever, A. Herman, and B. Arenkiel for their kind gift of viral preparations necessary to perform tracing experiments. This work was supported in part by the National Institute of Neurological Disorders and Stroke Grants NS077989 to MB, NS069777 and NS047085 to CSC, MH112768 to NJJ and CSC, and MH114032 to NJJ. RD was supported by a Zilkha Family Discovery Fellowship in neuroengineering.

Author contributions

AJH and NJJ designed experiments and analyzed the results; RD and MB designed and RD performed electrophysiological recordings. AJH, SR and ZY performed immunohistochemical and viral tracing experiments; AJH, CSC, and NJJ wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Supplementary material

429_2018_1652_MOESM1_ESM.eps (14.5 mb)
Validation of CRFR1-GFP and CRFR1-Cre transgenic mouse lines in the GPe. In situ hybridization (ish) for iCre mRNA (A, red), with Crfr1 mRNA (B, green) shows that neurons in the GPe express both iCre and CRFR1 in the CRFR1-Cre transgenic mouse (C, arrows). Immunolocalization of GFP (D, green) and CRFR1 protein (E, red) shows that CRFR1 protein is localized to GFP+ neurons in the GPe of CRFR1-GFP mice (F, arrows). Immunolocalization of tdTomato (G) and CRFR1 protein (H) shows that tdTomato-positive GPe neurons contain CRFR1 protein in the CRFR1-Cre transgenic mouse (I, arrows). Scalebar = 50µm (EPS 14849 KB)
429_2018_1652_MOESM2_ESM.eps (14.5 mb)
CRF is present in CRF neuron projections to the GPe. (A) In a mouse carrying the CRFR1-GFP, CRF-Cre and lsl-tom alleles, CRFR1 GPe neurons are green fluorescent. (B) Projections from CRF neurons are red fluorescent and course through the GPe. (C) Labeling sections from these mice with CRF antibodies reveals abundant puncta in the GPe. (D) In the merged image CRF staining aligns with tomato projections, indicating that CRF is present within CRF neuron projections. We observe small puncta positive for both CRF and CRF-cre:tomato (arrows), as well as larger structures filled with CRF (arrowheads). Scalebar = 25 µm (EPS 14849 KB)
429_2018_1652_MOESM3_ESM.eps (40 mb)
Retrograde tracing of stress-related nuclei from the GPe. Injection of fluorescently labeled retrobeads in the GPe identifies CRF neurons in the PVN, BSTld, and CeA that project to the GPe. In CRF-Cre; lsl-L10A-GFP mice in which CRF neurons are green fluorescent (A, D, G), injections of fluorobeads in the GPe traces neurons that project to the GPe (B, E, H). The merged image of the PVN (C) shows GPe projecting neurons in red, of which 3 are also positive for CRF-cre (arrows). In the merged image of the BSTld (F), we find GPe projecting neurons in the lateral aspects of the oval subnucleus (dashed oval), of which very few are CRF positive (arrow). In the merged image of the CeA (dashed outline), we see abundant accumulation of the retrograde tracer, in which a subpopulation are also positive for CRFR1-Cre transgene expression (arrows). Scalebar = 50µm (EPS 40963 KB)
429_2018_1652_MOESM4_ESM.eps (17.6 mb)
PTRV injections and quantification. An example low power micrograph shows that Cre-dependent helper virus injections (A, AAV-G/AAV-TVA-mChy) in Npas1-Cre transgenic mice cause Npas1 neurons across broad regions of the GPe to be red fluorescent. Secondary injections of PTRV (SADΔG-GFP) infect a small number of these neurons with rabies virus (arrows, yellow in C). The rabies virus transynaptically infects neurons connected to these starter neurons (green in C). Scalebar = 100µm. (D) Location of starter neurons in quantified PTRV experiments. The left side of each atlas diagram displays the positions of starter neurons in quantified CRFR1-Cre tracing experiments (red, blue and yellow). The right side of the brain displays the position of starter neurons in quantified Npas1-Cre tracing experiments (purple, orange, green). (left) Starter neurons in rostral regions of the GPe (0 to -0.5 mm AP from bregma) collapsed onto an atlas diagram of a brain section at -0.22 mm AP from bregma. (middle) Starter neurons in the central regions of the GPe (-0.5 to -0.8 mm AP to bregma) projected onto an atlas diagram of a coronal section at -0.7 mm from bregma. (right) Starter neurons in caudal regions of the GPe (-0.8 mm to -1.7 mm AP from bregma) collapsed onto an atlas diagram of a coronal section at -1.2mm AP from bregma. (E) Quantification of starter neurons and of traced neurons in the BSTld, PVN, and CeA. Three experiments were quantified for CRFR1-cre experiments (top), and three experiments were quantified for Npas1-cre experiments (bottom) (EPS 17990 KB)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Albert J. HuntJr.
    • 1
    • 4
  • Rajan Dasgupta
    • 2
    • 4
  • Shivakumar Rajamanickam
    • 1
  • Zhiying Jiang
    • 1
  • Michael Beierlein
    • 2
    • 4
  • C. Savio Chan
    • 3
  • Nicholas J. Justice
    • 1
    • 4
  1. 1.The Brown Foundation Institute of Molecular Medicine for the Prevention of Human Diseases, Center for Metabolic and Degenerative DiseasesUniversity of Texas Health Science Center at HoustonHoustonUSA
  2. 2.Department of Neurobiology and AnatomyMcGovern Medical SchoolHoustonUSA
  3. 3.Department of Physiology, Feinberg School of MedicineNorthwestern UniversityChicagoUSA
  4. 4.Graduate Program in NeuroscienceThe University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical SciencesHoustonUSA

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