Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Acute engagement of Gq-mediated signaling in the bed nucleus of the stria terminalis induces anxiety-like behavior

Molecular Psychiatry volume 23, pages 143–153 (2018)Cite this article

Subjects

Abstract

The bed nucleus of the stria terminalis (BNST) is a brain region important for regulating anxiety-related behavior in both humans and rodents. Here we used a chemogenetic strategy to investigate how engagement of G protein-coupled receptor (GPCR) signaling cascades in genetically defined GABAergic BNST neurons modulates anxiety-related behavior and downstream circuit function. We saw that stimulation of vesicular γ-aminobutyric acid (GABA) transporter (VGAT)-expressing BNST neurons using hM3Dq, but neither hM4Di nor rM3Ds designer receptors exclusively activated by a designer drug (DREADD), promotes anxiety-like behavior. Further, we identified that activation of hM3Dq receptors in BNST VGAT neurons can induce a long-term depression-like state of glutamatergic synaptic transmission, indicating DREADD-induced changes in synaptic plasticity. Further, we used DREADD-assisted metabolic mapping to profile brain-wide network activity following activation of Gq-mediated signaling in BNST VGAT neurons and saw increased activity within ventral midbrain structures, including the ventral tegmental area and hindbrain structures such as the locus coeruleus and parabrachial nucleus. These results highlight that Gq-mediated signaling in BNST VGAT neurons can drive downstream network activity that correlates with anxiety-like behavior and points to the importance of identifying endogenous GPCRs within genetically defined cell populations. We next used a microfluidics approach to profile the receptorome of single BNST VGAT neurons. This approach yielded multiple Gq-coupled receptors that are associated with anxiety-like behavior and several potential novel candidates for regulation of anxiety-like behavior. From this, we identified that stimulation of the Gq-coupled receptor 5-HT2CR in the BNST is sufficient to elevate anxiety-like behavior in an acoustic startle task. Together, these results provide a novel profile of receptors within genetically defined BNST VGAT neurons that may serve as therapeutic targets for regulating anxiety states and provide a blueprint for examining how G-protein-mediated signaling in a genetically defined cell type can be used to assess behavior and brain-wide circuit function.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. Griebel G, Holmes A . 50 years of hurdles and hope in anxiolytic drug discovery. Nat Rev Drug Discov 2013; 12: 667–687.

    Article  CAS  Google Scholar 

  2. Kessler RC, Chiu WT, Demler O, Walters EE . Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 2005; 62: 617.

    Article  Google Scholar 

  3. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE . Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 2005; 62: 593.

    Article  Google Scholar 

  4. Insel TR . Next-generation treatments for mental disorders. Sci Transl Med 2012; 4: 155ps19.

    Article  Google Scholar 

  5. Calhoon GG, Tye KM . Resolving the neural circuits of anxiety. Nat Neurosci 2015; 18: 1394–1404.

    Article  CAS  Google Scholar 

  6. Daniel SE, Rainnie DG . Stress modulation of opposing circuits in the bed nucleus of the stria terminalis. Neuropsychopharmacology 2016; 41: 103–125.

    Article  Google Scholar 

  7. Lebow MA, Chen A . Overshadowed by the amygdala: the bed nucleus of the stria terminalis emerges as key to psychiatric disorders. Mol Psychiatry 2016; 21: 450–463.

    Article  CAS  Google Scholar 

  8. Sun N, Cassell MD . Intrinsic GABAergic neurons in the rat central extended amygdala. J Comp Neurol 1993; 330: 381–404.

    Article  CAS  Google Scholar 

  9. Dong H-W, Swanson LW . Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. J Comp Neurol 2004; 468: 277–298.

    Article  Google Scholar 

  10. Dong H-W, Swanson LW . Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J Comp Neurol 2006; 494: 142–178.

    Article  Google Scholar 

  11. Straube T, Mentzel H-J, Miltner WHR . Waiting for spiders: brain activation during anticipatory anxiety in spider phobics. Neuroimage 2007; 37: 1427–1436.

    Article  Google Scholar 

  12. Mobbs D, Yu R, Rowe JB, Eich H, FeldmanHall O, Dalgleish T . Neural activity associated with monitoring the oscillating threat value of a tarantula. Proc Natl Acad Sci 2010; 107: 20582–20586.

    Article  CAS  Google Scholar 

  13. Mobbs D, Petrovic P, Marchant JL, Hassabis D, Weiskopf N, Seymour B et al. When fear is near: threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science 2007; 317: 1079–1083.

    Article  CAS  Google Scholar 

  14. Somerville LH, Whalen PJ, Kelley WM . Human bed nucleus of the stria terminalis indexes hypervigilant threat monitoring. Biol Psychiatry.; 2010; 68: 416–424.

    Article  Google Scholar 

  15. Kim S-Y, Adhikari A, Lee SY, Marshel JH, Kim CK, Mallory CS et al. Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 2013; 496: 219–223.

    Article  CAS  Google Scholar 

  16. Jennings JH, Sparta DR, Stamatakis AM, Ung RL, Pleil KE, Kash TL et al. Distinct extended amygdala circuits for divergent motivational states. Nature 2016; 496: 224–228.

    Article  Google Scholar 

  17. Yassa MA, Hazlett RL, Stark CEL, Hoehn-Saric R . Functional MRI of the amygdala and bed nucleus of the stria terminalis during conditions of uncertainty in generalized anxiety disorder. J Psychiatr Res 2012; 46: 1045–1052.

    Article  Google Scholar 

  18. Fox AS, Shelton SE, Oakes TR, Davidson RJ, Kalin NH . Trait-like brain activity during adolescence predicts anxious temperament in primates. PLoS One 2008; 3: e2570.

    Article  Google Scholar 

  19. Kalin NH, Shelton SE, Fox AS, Oakes TR, Davidson RJ . Brain regions associated with the expression and contextual regulation of anxiety in primates. Biol Psychiatry 2005; 58: 796–804.

    Article  Google Scholar 

  20. Lee Y, Davis M . Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. J Neurosci 1997; 17: 6434–6446.

    Article  CAS  Google Scholar 

  21. Walker DL, Davis M . Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 1997; 17: 9375–9383.

    Article  CAS  Google Scholar 

  22. Waddell J, Morris RW, Bouton ME . Effects of bed nucleus of the stria terminalis lesions on conditioned anxiety: aversive conditioning with long-duration conditional stimuli and reinstatement of extinguished fear. Behav Neurosci 2006; 120: 324–336.

    Article  Google Scholar 

  23. Kash TL . The role of biogenic amine signaling in the bed nucleus of the stria terminals in alcohol abuse. Alcohol 2012; 46: 303–308.

    Article  CAS  Google Scholar 

  24. Kash TL, Pleil KE, Marcinkiewcz CA, Lowery-Gionta EG, Crowley N, Mazzone C et al. Neuropeptide regulation of signaling and behavior in the BNST. Mol Cells 2015; 38: 1–13.

    Article  Google Scholar 

  25. Cecchi M, Khoshbouei H, Javors M, Morilak DA . Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuroscience 2002; 112: 13–21.

    Article  CAS  Google Scholar 

  26. Walker DL, Miles LA, Davis M . Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog Neuropsychopharmacol Biol Psychiatry.; 2009; 33: 1291–1308.

    Article  CAS  Google Scholar 

  27. Walker D, Yang Y, Ratti E, Corsi M, Trist D, Davis M . Differential effects of the CRF-R1 antagonist GSK876008 on fear-potentiated, light- and CRF-enhanced startle suggest preferential involvement in sustained vs phasic threat responses. Neuropsychopharmacology 2009; 34: 1533–1542.

    Article  CAS  Google Scholar 

  28. Hammack SE, Cheung J, Rhodes KM, Schutz KC, Falls W a, Braas KM et al. Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology 2009; 34: 833–843.

    Article  CAS  Google Scholar 

  29. Levita L, Hammack SE, Mania I, Li X-Y, Davis M, Rainnie DG . 5-hydroxytryptamine1a-likereceptor activation in the bed nucleus of the stria terminalis: electrophysiological and behavioral studies. Neuroscience 2004; 128: 583–596.

    Article  CAS  Google Scholar 

  30. Fox JH, Hammack SE, Falls WA . Exercise is associated with reduction in the anxiogenic effect of mCPP on acoustic startle. Behav Neurosci 2008; 122: 943–948.

    Article  Google Scholar 

  31. Heisler LK, Zhou L, Bajwa P, Hsu J, Tecott LH . Serotonin 5-HT(2C) receptors regulate anxiety-like behavior. Genes Brain Behav 2007; 6: 491–496.

    Article  CAS  Google Scholar 

  32. Vong L, Ye C, Yang Z, Choi B, Chua S, Lowell BB . Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 2011; 71: 142–154.

    Article  CAS  Google Scholar 

  33. Krashes MJ, Shah BP, Madara JC, Olson DP, Strochlic DE, Garfield AS et al. An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger. Nature 2014; 507: 238–242.

    Article  CAS  Google Scholar 

  34. Franklin KBJ, Paxinos G . The Mouse Brain in Stereotaxic Coordinates, Compact, 3rd edn. Elsevier: New York, NY, USA, 2008.

    Google Scholar 

  35. Michaelides M, Pascau J, Gispert JD, Delis F, Grandy DK, Wang GJ et al. Dopamine D4 receptors modulate brain metabolic activity in the prefrontal cortex and cerebellum at rest and in response to methylphenidate. Eur J Neurosci 2010; 32: 668–676.

    Article  Google Scholar 

  36. Urban DJ, Zhu H, Marcinkiewcz CA, Michaelides M, Oshibuchi H, Rhea D et al. Elucidation of the behavioral program and neuronal network encoded by dorsal raphe serotonergic neurons. Neuropsychopharmacology 2015; 41: 1404–1415.

    Article  Google Scholar 

  37. Hur EE, Zaborszky L . Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization. J Comp Neurol 2005; 483: 351–373.

    Article  Google Scholar 

  38. Poulin J-F, Arbour D, Laforest S, Drolet G . Neuroanatomical characterization of endogenous opioids in the bed nucleus of the stria terminalis. Prog Neuropsychopharmacol Biol Psychiatry 2009; 33: 1356–1365.

    Article  CAS  Google Scholar 

  39. Kudo T, Uchigashima M, Miyazaki T, Konno K, Yamasaki M, Yanagawa Y et al. Three types of neurochemical projection from the bed nucleus of the stria terminalis to the ventral tegmental area in adult mice. J Neurosci 2012; 32: 18035–18046.

    Article  CAS  Google Scholar 

  40. Armbruster BN, Li X, Pausch MH, Herlitze S, Roth BL . Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc Natl Acad Sci USA 2007; 104: 5163–5168.

    Article  Google Scholar 

  41. Krashes MJ, Koda S, Ye C, Rogan SC, Adams AC, Cusher DS et al. Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J Clin Invest 2011; 121: 1424–1428.

    Article  CAS  Google Scholar 

  42. Alexander GM, Rogan SC, Abbas AI, Armbruster BN, Pei Y, Allen JA et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 2009; 63: 27–39.

    Article  CAS  Google Scholar 

  43. Yiu AP, Mercaldo V, Yan C, Richards B, Rashid AJ, Hsiang H-LL et al. Neurons are recruited to a memory trace based on relative neuronal excitability immediately before training. Neuron 2014; 83: 722–735.

    Article  CAS  Google Scholar 

  44. Grueter BA, Gosnell HB, Olsen CM, Schramm-Sapyta NL, Nekrasova T, Landreth GE et al. Extracellular-signal regulated kinase 1-dependent metabotropic glutamate receptor 5-induced long-term depression in the bed nucleus of the stria terminalis is disrupted by cocaine administration. J Neurosci 2006; 26: 3210–3219.

    Article  CAS  Google Scholar 

  45. McElligott Z a, Klug JR, Nobis WP, Patel S, Grueter BA, Kash TL et al. Distinct forms of Gq-receptor-dependent plasticity of excitatory transmission in the BNST are differentially affected by stress. Proc Natl Acad Sci 2010; 107: 2271–2276.

    Article  CAS  Google Scholar 

  46. McElligott ZA, Winder DG . Alpha1-adrenergic receptor-induced heterosynaptic long-term depression in the bed nucleus of the stria terminalis is disrupted in mouse models of affective disorders. Neuropsychopharmacology 2008; 33: 2313–2323.

    Article  CAS  Google Scholar 

  47. Michaelides M, Anderson SAR, Ananth M, Smirnov D, Thanos PK, Neumaier JF et al. Whole-brain circuit dissection in free-moving animals reveals cell-specific mesocorticolimbic networks. J Clin Invest 2013; 123: 5342–5350.

    Article  CAS  Google Scholar 

  48. Anderson SAR, Michaelides M, Zarnegar P, Ren Y, Fagergren P, Thanos PK et al. Impaired periamygdaloid-cortex prodynorphin is characteristic of opiate addiction and depression. J Clin Invest 2013; 123: 5334–5341.

    Article  CAS  Google Scholar 

  49. Burghardt NS, Sullivan GM, McEwen BS, Gorman JM, LeDoux JE . The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biol Psychiatry 2004; 55: 1171–1178.

    Article  CAS  Google Scholar 

  50. Ravinder S, Burghardt NS, Brodsky R, Bauer EP, Chattarji S . A role for the extended amygdala in the fear-enhancing effects of acute selective serotonin reuptake inhibitor treatment. Transl Psychiatry 2013; 3: e209.

    Article  CAS  Google Scholar 

  51. Marcinkiewcz CA, Mazzone CM, D’Agostino G, Halladay LR, Hardaway JA, DiBerto JF et al. Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala. Nature 2016; 537: 97–101.

    Article  CAS  Google Scholar 

  52. Nakajima K, Cui Z, Li C, Meister J, Cui Y, Fu O et al. Gs-coupled GPCR signalling in AgRP neurons triggers sustained increase in food intake. Nat Commun 2016; 7: 10268.

    Article  CAS  Google Scholar 

  53. Pleil KE, Rinker JA, Lowery-Gionta EG, Mazzone CM, McCall NM, Kendra AM et al. NPY signaling inhibits extended amygdala CRF neurons to suppress binge alcohol drinking. Nat Neurosci 2015; 18: 545–552.

    Article  CAS  Google Scholar 

  54. Kash TL, Winder DG . Neuropeptide Y and corticotropin-releasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis. Neuropharmacology 2006; 51: 1013–1022.

    Article  CAS  Google Scholar 

  55. Valdez GR, Koob GF . Allostasis and dysregulation of corticotropin-releasing factor and neuropeptide Y systems: implications for the development of alcoholism. Pharmacol Biochem Behav 2004; 79: 671–689.

    Article  CAS  Google Scholar 

  56. Heilig M . The NPY system in stress, anxiety and depression. Neuropeptides 2004; 38: 213–224.

    Article  CAS  Google Scholar 

  57. Heilig M, Koob GF . A key role for corticotropin-releasing factor in alcohol dependence. Trends Neurosci 2007; 30: 399–406.

    Article  CAS  Google Scholar 

  58. López AJ, Kramár E, Matheos DP, White AO, Kwapis J, Vogel-Ciernia A et al. Promoter-specific effects of DREADD modulation on hippocampal synaptic plasticity and memory formation. J Neurosci 2016; 36: 3588–3599.

    Article  Google Scholar 

  59. Glangetas C, Girard D, Groc L, Marsicano G, Chaouloff F, Georges F . Stress switches cannabinoid type-1 (CB1) receptor-dependent plasticity from LTD to LTP in the bed nucleus of the stria terminalis. J Neurosci 2013; 33: 19657–19663.

    Article  Google Scholar 

  60. Sehlmeyer C, Schöning S, Zwitserlood P, Pfleiderer B, Kircher T, Arolt V et al. Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One 2009; 4: e5865.

    Article  Google Scholar 

  61. Nagai M, Kishi K, Kato S . Insular cortex and neuropsychiatric disorders: a review of recent literature. Eur Psychiatry 2007; 22: 387–394.

    Article  CAS  Google Scholar 

  62. Shackman AJ, Fox AS . Contributions of the central extended amygdala to fear and anxiety. J Neurosci 2016; 36: 8050–8063.

    Article  CAS  Google Scholar 

  63. Gungor NZ, Pare D . Functional heterogeneity in the bed nucleus of the stria terminalis. J Neurosci 2016; 36: 8038–8049.

    Article  CAS  Google Scholar 

  64. Shackman AJ, Fox AS, Oler JA, Shelton SE, Davidson RJ, Kalin NH . Neural mechanisms underlying heterogeneity in the presentation of anxious temperament. Proc Natl Acad Sci 2013; 110: 6145–6150.

    Article  CAS  Google Scholar 

  65. Awwad HO, Gonzalez LP, Tompkins P, Lerner M, Brackett DJ, Awasthi V et al. Blast overpressure waves induce transient anxiety and regional changes in cerebral glucose metabolism and delayed hyperarousal in rats. Front Neurol 2015; 6: 132.

    Article  Google Scholar 

  66. Liu M-L, Liang F-R, Zeng F, Tang Y, Lan L, Song W-Z . Cortical-limbic regions modulate depression and anxiety factors in functional dyspepsia: a PET-CT study. Ann Nucl Med 2012; 26: 35–40.

    Article  CAS  Google Scholar 

  67. Pleil KE, Helms CM, Sobus JR, Daunais JB, Grant KA, Kash TL . Effects of chronic alcohol consumption on neuronal function in the non-human primate BNST. Addict Biol 2015; 21: 1151–1167.

    Article  Google Scholar 

  68. Marcinkiewcz C a, Dorrier CE, Lopez AJ, Kash TL . Ethanol induced adaptations in 5-HT2c receptor signaling in the bed nucleus of the stria terminalis: implications for anxiety during ethanol withdrawal. Neuropharmacology 2015; 89: 157–167.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr Francisco Javier Rubio Gallego for providing the protocol used for single-cell dissociations. FACS and Fluidigm experiments were conducted by the UNC Advanced Analytics Core (Center for GI Biology and Disease; P30 DK034987). This work was supported by the National Institute on Drug Abuse (NIDA; DA015446, DA033660, DA030359). MM was supported by the NIDA Postdoctoral Training Program at Icahn School of Medicine at Mount Sinai (DA007135). JAH was funded by MH076694. CMM was funded by F31 AA023440 from the National Institute on Alcohol Abuse and Alcoholism. TLK was funded by P60 AA011605, R01 AA019454, U01 AA020911 and U01 MH105892. JMM is supported by an Institutional Postdoctoral NRSA T32 AA007573. ZAM was funded by K01 AA023555 and the Alcohol Beverage Medical Research Fund. The acoustic startle experiment was funded by MH080935 (to SEH).

Author information

Authors and Affiliations

  1. Neurobiology Curriculum, University of North Carolina, Chapel Hill, NC, USA

    C M Mazzone

  2. Laboratory of Molecular Neurophysiology, Bowles Center for Alcohol Studies, University of North Carolina School of Medicine, Chapel Hill, NC, USA

    C M Mazzone, D Pati, J DiBerto, G Tipton, K Duffy, J M McKlveen, J A Hardaway & T L Kash

  3. Fishberg Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    M Michaelides & Y L Hurd

  4. Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    M Michaelides & Y L Hurd

  5. Biobehavioral Imaging and Molecular Neuropsychopharmacology Unit, Neuroimaging Research Branch, National Institute on Drug Abuse, Baltimore, MD, USA

    M Michaelides

  6. Department of Psychology, University of Vermont, Burlington, VT, USA

    J H Fox, W A Falls & S E Hammack

  7. Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC, USA

    C Anderson

  8. Department of Medicine, University of North Carolina, Chapel Hill, NC, USA

    S T Magness

  9. Department of Cell Biology and Physiology, and Biomedical Engineering, University of North Carolina, Chapel Hill, NC, USA

    S T Magness

  10. Department of Psychiatry, University of North Carolina, Chapel Hill, NC, USA

    Z A McElligott

  11. Department of Pharmacology, School of Medicine, University of North Carolina at, Chapel Hill, NC, USA

    T L Kash

Authors
  1. C M Mazzone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D Pati
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M Michaelides
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J DiBerto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J H Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. G Tipton
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. K Duffy
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. J M McKlveen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. J A Hardaway
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. S T Magness
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. W A Falls
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. S E Hammack
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Z A McElligott
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Y L Hurd
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. T L Kash
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T L Kash.

Ethics declarations

Competing interests

MM owns stock in Metis Laboratories. The remaining authors declare no conflict of interest.

Additional information

Supplementary Information accompanies the paper on the Molecular Psychiatry website

Supplementary information

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mazzone, C., Pati, D., Michaelides, M. et al. Acute engagement of Gq-mediated signaling in the bed nucleus of the stria terminalis induces anxiety-like behavior. Mol Psychiatry 23, 143–153 (2018). https://doi.org/10.1038/mp.2016.218

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/mp.2016.218

This article is cited by

Search

Advanced search

Quick links