Corticotropin-releasing factor neurons in the bed nucleus of the stria terminalis exhibit sex-specific pain encoding in mice
Open accessPublished version of a preprint
Abstract
The bed nucleus of the stria terminalis (BNST) plays an emerging role in pain regulation. Pharmacological studies have found that inhibiting corticotropin-releasing factor (CRF) signaling in the BNST can selectively mitigate the sensory and affective-motivational components of pain. However, mechanistic insight on the source of CRF that drives BNST responses to these harmful experiences remains unknown. In the present study, we used a series of genetic approaches to show that CRF in the BNST is engaged in the processing and modulation of pain. We conducted cell-type specific in vivo calcium imaging in CRF-Cre mice and found robust and synchronized recruitment of BNST CRF neurons during acute exposures to noxious heat. Distinct patterns of recruitment were observed by sex, as the magnitude and timing of heat responsive activity in BNST CRF neurons differed for male and female mice. We then used a viral approach in Floxed-CRF mice to selectively reduce CRF expression in the BNST and found it decreased nociceptive sensitivity for both sexes and increased paw attending for females. Together, these findings reveal that CRF in the BNST influences multiple facets of the pain experience to impact the sex-specific expression of pain-related behaviors.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The BNST exhibits heterogeneity in neural responses, even within genetically defined cell populations.
“This is further complicated by the fact that the BNST exhibits heterogeneity in neural responses, even within genetically defined cell populations (83–85).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [83]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
SciPy 1.0: fundamental algorithms for scientific computing in Python
Virtanen, P., Gommers, R., Oliphant, T. E., Haberland, M., Reddy, T., Cournapeau, D., Burovski, E., Peterson, P., Weckesser, W., Bright, J., et al. (2020) · Nature Methods · doi:10.1038/s41592-019-0686-2 · Cited by 38,430 · see citing works
SciPy 1.0: fundamental algorithms for scientific computing in Python
Virtanen, P., Gommers, R., Oliphant, T. E., Haberland, M., Reddy, T., Cournapeau, D., Burovski, E., Peterson, P., Weckesser, W., Bright, J., et al. (2019) · Apollo - University of Cambridge Repository · doi:10.17863/cam.64134 · Cited by 10,460 · see citing works
Animal research: Reporting <i>in vivo</i> experiments: The ARRIVE guidelines
Kilkenny, C., Browne, W., Cuthill, I. C., Emerson, M., & Altman, D. G. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00872.x · Cited by 3,625 · see citing works
Sex differences in pain: a brief review of clinical and experimental findings
Bartley, E. J., & Fillingim, R. B. (2013) · British Journal of Anaesthesia · doi:10.1093/bja/aet127 · Cited by 2,168 · see citing works
Sex differences in pain and pain inhibition: multiple explanations of a controversial phenomenon
Mogil, J. S. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3360 · Cited by 1,065 · see citing works
Topography of projections from amygdala to bed nuclei of the stria terminalis
Dong, H.-W., Petrovich, G. D., & Swanson, L. W. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00079-0 · Cited by 714 · see citing works
Qualitative sex differences in pain processing: emerging evidence of a biased literature
Mogil, J. S. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0310-6 · Cited by 691 · see citing works
An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger
Krashes, M. J., Shah, B. P., Madara, J. C., Olson, D. P., Strochlic, D. E., Garfield, A. S., Vong, L., Pei, H., Watabe-Uchida, M., Uchida, N., et al. (2014) · Nature · doi:10.1038/nature12956 · Cited by 603 · see citing works
Central circuits mediating patterned autonomic activity during active vs. passive emotional coping
Bandler, R., Keay, K. A., Floyd, N., & Price, J. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00313-0 · Cited by 582 · see citing works
Bonin, R. P., Bories, C., & Koninck, Y. D. (2014) · Molecular Pain · doi:10.1186/1744-8069-10-26 · Cited by 468 · see citing works
Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala
Marcinkiewcz, C. A., Mazzone, C. M., D’Agostino, G., Halladay, L. R., Hardaway, J. A., DiBerto, J. F., Navarro, M., Burnham, N., Cristiano, C., Dorrier, C. E., et al. (2016) · Nature · doi:10.1038/nature19318 · Cited by 456 · see citing works
Self-citationCummings, S., Elde, R., Ells, J., & Lindall, A. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-07-01355.1983 · Cited by 414 · see citing works
An amygdalar neural ensemble that encodes the unpleasantness of pain
Corder, G. F., Ahanonu, B., Grewe, B. F., Wang, D., Schnitzer, M. J., & Scherrer, G. (2019) · Science · doi:10.1126/science.aap8586 · Cited by 406 · see citing works
Sex-Based Differences in Pain Perception and Treatment
Paller, C. J., Campbell, C. M., Edwards, R. R., & Dobs, A. S. (2009) · Pain Medicine · doi:10.1111/j.1526-4637.2008.00558.x · Cited by 396 · see citing works
Cognitive Impairment in Pain through Amygdala-Driven Prefrontal Cortical Deactivation
Ji, G., Sun, H., Fu, Y., Li, Z., Pais-Vieira, M., Galhardo, V., & Neugebauer, V. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0225-10.2010 · Cited by 387 · see citing works
Ju, G., & Swanson, L. W. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902800409 · Cited by 359 · see citing works
Neural ensemble dynamics underlying a long-term associative memory
Grewe, B. F., Gründemann, J., Kitch, L. J., Lecoq, J. A., Parker, J. G., Marshall, J. D., Larkin, M. C., Jercog, P. E., Grenier, F., Li, J. Z., et al. (2017) · Nature · doi:10.1038/nature21682 · Cited by 351 · see citing works
Human Bed Nucleus of the Stria Terminalis Indexes Hypervigilant Threat Monitoring
Somerville, L. H., Whalen, P. J., & Kelley, W. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.04.002 · Cited by 351 · see citing works
Corder, G. F., Tawfik, V. L., Wang, D., Sypek, E. I., Low, S. A., Dickinson, J. R., Sotoudeh, C., Clark, J. D., Barres, B. A., Bohlen, C. J., et al. (2017) · Nature Medicine · doi:10.1038/nm.4262 · Cited by 347 · see citing works
Sakanaka, M., Shibasaki, T., & Lederis, K. (1986) · Brain Research · doi:10.1016/0006-8993(86)91332-6 · Cited by 337 · see citing works
Moga, M. M., Saper, C. B., & Gray, T. S. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902830302 · Cited by 333 · see citing works
The human BNST: functional role in anxiety and addiction
Avery, S. N., Clauss, J. A., & Blackford, J. U. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.185 · Cited by 331 · see citing works
Schäfer, M., Carter, L., & Stein, C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.10.4219 · Cited by 293 · see citing works
Chronic Pain and Chronic Stress: Two Sides of the Same Coin?
Abdallah, C. G., & Geha, P. (2017) · Chronic Stress · doi:10.1177/2470547017704763 · Cited by 286 · see citing works
Giardino, W. J., Eban-Rothschild, A., Christoffel, D. J., Li, S.-B., Malenka, R. C., & de Lecea, L. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0198-x · Cited by 252 · see citing works
The role of corticotropin‐releasing factor in pain and analgesia
Lariviere, W., & Melzack, R. (2000) · Pain · doi:10.1016/s0304-3959(99)00193-1 · Cited by 232 · see citing works
Pain and analgesia: the value of salience circuits
Borsook, D., Edwards, R., Elman, I., Becerra, L., & Levine, J. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.02.003 · Cited by 215 · see citing works
Stress Modulation of Opposing Circuits in the Bed Nucleus of the Stria Terminalis
Daniel, S., & Rainnie, D. G. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.178 · Cited by 213 · see citing works
Sahuque, L. L., Kullberg, E. F., Mcgeehan, A. J., Kinder, J. R., Hicks, M. P., Blanton, M. G., Janak, P. H., & Olive, M. F. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0362-y · Cited by 207 · see citing works
A Central Amygdala CRF Circuit Facilitates Learning about Weak Threats
Sanford, C. A., Soden, M. E., Baird, M. A., Miller, S. M., Schulkin, J. A., Palmiter, R. D., Clark, M., & Zweifel, L. S. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.034 · Cited by 199 · see citing works
Ju, G., Swanson, L. W., & Simerly, R. B. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902800410 · Cited by 197 · see citing works
NPY signaling inhibits extended amygdala CRF neurons to suppress binge alcohol drinking
Pleil, K. E., Rinker, J. A., Lowery-Gionta, E. G., Mazzone, C. M., McCall, N. M., Kendra, A. M., Olson, D. P., Lowell, B. B., Grant, K. A., Thiele, T. E., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3972 · Cited by 195 · see citing works
Self-citationSex differences in stress responses: a critical role for corticotropin-releasing factor
Bangasser, D. A., & Wiersielis, K. (2018) · HORMONES · doi:10.1007/s42000-018-0002-z · Cited by 193 · see citing works
del Abril, A., Segovia, S., & Guillamón, A. (1987) · Developmental Brain Research · doi:10.1016/0165-3806(87)90110-6 · Cited by 184 · see citing works
The central amygdala controls learning in the lateral amygdala
Yu, K., Ahrens, S., Zhang, X., Schiff, H. C., Ramakrishnan, C., Fenno, L. E., Deisseroth, K. A., Zhao, F., Luo, M., Gong, L., et al. (2017) · Nature Neuroscience · doi:10.1038/s41593-017-0009-9 · Cited by 176 · see citing works
Dabrowska, J., Hazra, R., Guo, J., DeWitt, S., & Rainnie, D. G. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00156 · Cited by 163 · see citing works
General anesthetics activate a potent central pain-suppression circuit in the amygdala
Hua, T., Chen, B., Lu, D., Sakurai, K., Zhao, S., Han, B.-X., Kim, J., Yin, L., Chen, Y., Lu, J., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0632-8 · Cited by 151 · see citing works
Morin, S. M., LING, N. C., Liu, X.-J., Kahl, S. D., & Gehlert, D. R. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00732-5 · Cited by 149 · see citing works
Schäfer, M., Mousa, S. A., Zhang, Q., Carter, L., & Stein, C. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.12.6096 · Cited by 132 · see citing works
Diffusion tensor microscopy of the intervertebral disc anulus fibrosus
Hsu, E. W., & Setton, L. A. (1999) · Magnetic Resonance in Medicine · doi:10.1002/(sici)1522-2594(199905)41:5 · Cited by 127 · see citing works
Corticotropin-Releasing Factor Disrupts Sensory Responses of Brain Noradrenergic Neurons
Valentino, R. J., & Foote, S. L. (2008) · Neuroendocrinology · doi:10.1159/000124700 · Cited by 125 · see citing works
Han, T. M., & De Vries, G. J. (2003) · Journal of Neurobiology · doi:10.1002/neu.10157 · Cited by 116 · see citing works
Dissecting the Anticipation of Aversion Reveals Dissociable Neural Networks
Grupe, D. W., Oathes, D. J., & Nitschke, J. B. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs175 · Cited by 115 · see citing works
Sink, K. S., Walker, D. L., Freeman, S. M., Flandreau, E. I., Ressler, K. J., & Davis, M. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.188 · Cited by 108 · see citing works
Spinal pain suppression mechanisms may differ for phasic and tonic pain
Ryan, S. M., Watkins, L. R., Mayer, D. J., & Maier, S. F. (1985) · Brain Research · doi:10.1016/0006-8993(85)90582-7 · Cited by 102 · see citing works
Loss of hypothalamic corticotropin-releasing hormone markedly reduces anxiety behaviors in mice
Zhang, R., Asai, M., Mahoney, C. E., Joachim, M., Shen, Y., Gunner, G., & Majzoub, J. A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.136 · Cited by 97 · see citing works
Pomrenze, M. B., Giovanetti, S. M., Maiya, R., Gordon-Fennell, A., Kreeger, L. J., & Messing, R. O. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.08.083 · Cited by 93 · see citing works
Corticotropin-releasing factor (CRF) produces analgesia in humans and rats
Hargreaves, K., Mueller, G. P., Dubner, R. A., Goldstein, D. S., & Dionne, R. A. (1987) · Brain Research · doi:10.1016/0006-8993(87)90550-6 · Cited by 91 · see citing works
Tran, L., Schulkin, J. A., & Meerveld, B. G. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.117 · Cited by 82 · see citing works
Funabashi, T., Kawaguchi, M., Furuta, M., Fukushima, A., & Kimura, F. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00055-6 · Cited by 79 · see citing works
Herrmann, M. J., Boehme, S., Becker, M. P. I., Tupak, S. V., Guhn, A., Schmidt, B., Brinkmann, L., & Straube, T. (2015) · Human Brain Mapping · doi:10.1002/hbm.23088 · Cited by 79 · see citing works
Levine, O. B., Skelly, M. J., Miller, J. D., Rivera-Irizarry, J. K., Rowson, S. A., DiBerto, J. F., Rinker, J. A., Thiele, T. E., Kash, T. L., & Pleil, K. E. (2021) · Nature Communications · doi:10.1038/s41467-021-25368-y · Cited by 78 · see citing works
Self-citationDabrowska, J., Martinon, D., Moaddab, M., & Rainnie, D. G. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12442 · Cited by 75 · see citing works
Rodriguez-Romaguera, J., Ung, R. L., Nomura, H., Otis, J. M., Basiri, M. L., Namboodiri, V. M. K., Zhu, X., Robinson, J. E., van den Munkhof, H. E., McHenry, J. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108362 · Cited by 75 · see citing works
Self-citationTanaka, G., Shigeta, M., Komatsuzawa, H., Sugai, M., Suginaka, H., & Usui, T. (1999) · Chemotherapy · doi:10.1159/000007162 · Cited by 72 · see citing works
Deyama, S., Katayama, T., Ohno, A., Nakagawa, T., Kaneko, S., Yamaguchi, T., Yoshioka, M., & Minami, M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1480-08.2008 · Cited by 71 · see citing works
Uchida, K., Otsuka, H., Morishita, M., Tsukahara, S., Sato, T., Sakimura, K., & Itoi, K. (2019) · Biology of Sex Differences · doi:10.1186/s13293-019-0221-2 · Cited by 70 · see citing works
Ide, S., Hara, T., Ohno, A., Tamano, R., Koseki, K., Naka, T., Maruyama, C., Kaneda, K., Yoshioka, M., & Minami, M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4278-12.2013 · Cited by 68 · see citing works
Brinkmann, L., Buff, C., Feldker, K., Tupak, S. V., Becker, M. P. I., Herrmann, M. J., & Straube, T. (2017) · Psychological Medicine · doi:10.1017/s0033291717001192 · Cited by 68 · see citing works
Mousa, S. A., Schäfer, M., Mitchell, W. M., Hassan, A. H. S., & Stein, C. (1996) · European Journal of Pharmacology · doi:10.1016/0014-2999(96)00440-2 · Cited by 68 · see citing works
Crown, E. D., King, T. E., Meagher, M. W., & Grau, J. W. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.3.561 · Cited by 65 · see citing works
Bangasser, D. A., & Shors, T. J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0831-08.2008 · Cited by 64 · see citing works
Corticotropin-releasing factor inhibits neurogenic plasma extravasation in the rat paw.
Wei, E. T., Kiang, J. G., Buchan, P., & Smith, T. W. (1986) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)24327-0 · Cited by 63 · see citing works
Deyama, S., Nakagawa, T., Kaneko, S., Uehara, T., & Minami, M. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.021 · Cited by 59 · see citing works
Rouwette, T., Klemann, C. J. H. M., Gaszner, B., Scheffer, G. J., Roubos, E. W., Scheenen, W. J. J. M., Vissers, K. C. P., & Kozicz, T. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.054 · Cited by 54 · see citing works
Divergent role for CRF1 and CRF2 receptors in the modulation of visceral pain
Nijsen, M., Ongenae, N., Meulemans, A., & Coulie, B. J. (2005) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2005.00644.x · Cited by 52 · see citing works
Experimental neuropathy increases limbic forebrain CRF
Rouwette, T., Vanelderen, P., de Reus, M., Loohuis, N. F. M. O., Giele, J. L. P., van Egmond, J., Scheenen, W. J. J. M., Scheffer, G. J., Roubos, E. W., Vissers, K. C. P., et al. (2011) · European Journal of Pain · doi:10.1016/j.ejpain.2011.05.016 · Cited by 48 · see citing works
Mousa, S. A., Bopaiah, C., Richter, J. F., Yamdeu, R.-S., & Schäfer, M. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301393 · Cited by 46 · see citing works
A Novel Transgenic Mouse for Gene-Targeting Within Cells That Express Corticotropin-Releasing Factor
Martin, E. I., Ressler, K. J., Jasnow, A. M., Dabrowska, J., Hazra, R., Rainnie, D. G., Nemeroff, C. B., & Owens, M. J. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.01.026 · Cited by 45 · see citing works
Frost, N. A., Haggart, A., & Sohal, V. S. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001235 · Cited by 43 · see citing works
Deyama, S., Katayama, T., Kondoh, N., Nakagawa, T., Kaneko, S., Yamaguchi, T., Yoshioka, M., & Minami, M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.08.024 · Cited by 42 · see citing works
Cui, X.-Y., Lundeberg, T., & Yu, L. (2003) · Brain Research · doi:10.1016/j.brainres.2003.09.050 · Cited by 38 · see citing works
Corticotropin releasing factor impairs sustained attention in male and female rats
Cole, R. D., Kawasumi, Y., Parikh, V., & Bangasser, D. A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.08.023 · Cited by 33 · see citing works
Sinniger, V., Porcher, C., Mouchet, P., Juhem, A., & Bonaz, B. L. (2004) · Pain · doi:10.1016/j.pain.2004.05.014 · Cited by 33 · see citing works
Klampfl, S. M., Brunton, P. J., Bayerl, D. S., & Bosch, O. J. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.11.015 · Cited by 32 · see citing works
Lautenbacher, S., Roscher, S., Kohl, G., Vedder, H., & Krieg, J.-C. (1999) · Pain · doi:10.1016/s0304-3959(99)00072-x · Cited by 32 · see citing works
Takahashi, D., Asaoka, Y., Kimura, K., Hara, R., Arakaki, S., Sakasai, K., Suzuki, H., Yamauchi, N., Nomura, H., Amano, T., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.3047-18.2019 · Cited by 30 · see citing works
Kita, A., Imano, K., & Nakamura, H. (1993) · European Journal of Pharmacology · doi:10.1016/0014-2999(93)90284-o · Cited by 29 · see citing works
Janitzky, K., Peine, A., Kröber, A., Yanagawa, Y., Schwegler, H., & Roskoden, T. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.06.020 · Cited by 27 · see citing works
Minami, M., & Ide, S. (2015) · Current Molecular Medicine · doi:10.2174/1566524015666150303002336 · Cited by 26 · see citing works
The role of the bed nucleus of the stria terminalis in pain-induced aversive motivation
Minami, M. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.10.003 · Cited by 23 · see citing works
The role of the anteriolateral bed nucleus of the stria terminalis in stress-induced nociception
Tran, L., Wiskur, B. J., & Meerveld, B. G. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00501.2011 · Cited by 22 · see citing works
Jenks, S. K., Zhang, S., Li, C.-S. R., & Hu, S. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.12.017 · Cited by 22 · see citing works
Song, Z., & Takemori, A. E. (1990) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)23082-8 · Cited by 15 · see citing works
Kaneko, T., Kaneda, K., Ohno, A., Takahashi, D., Hara, T., Amano, T., Ide, S., Yoshioka, M., & Minami, M. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13419 · Cited by 14 · see citing works
How Accurate Appraisal of Behavioral Costs and Benefits Guides Adaptive Pain Coping
Gandhi, W., Morrison, I., & Schweinhardt, P. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00103 · Cited by 14 · see citing works
Smithers, H. E., Terry, J. R., Brown, J. T., & Randall, A. D. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100143 · Cited by 13 · see citing works
Hara, R., Asaoka, Y., Takahashi, D., Nomura, H., Amano, T., & Minami, M. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.134958 · Cited by 7 · see citing works
Xu, W.-X. (2017) · Gastroenterology & Hepatology Open Access · doi:10.15406/ghoa.2017.06.00207 · Cited by 3 · see citing works
Flagged first, then by citations
1 of the 91 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Sex differences in fear responses: Neural circuits
Bauer, E. P. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109298 · Cited by 84 · see citing works
The Raphe Dopamine System: Roles in Salience Encoding, Memory Expression, and Addiction
Lin, R., Liang, J., & Luo, M. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.01.002 · Cited by 36 · see citing works
Sexual differentiation of neural mechanisms of stress sensitivity during puberty
Wright, E. C., Luo, P. X., Zakharenkov, H. C., Serna Godoy, A., Lake, A. A., Prince, Z. D., Sekar, S., Culkin, H. I., Ramirez, A. V., Dwyer, T., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2306475120 · Cited by 34 · see citing works
Zhang, Y., Ma, H., Bai, Y., Hou, X., Yang, Y., Wang, G., & Li, Y. (2024) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.4c00125 · Cited by 25 · see citing works
Distinct Encoding of Reward and Aversion by Peptidergic BNST Inputs to the VTA
Soden, M. E., Yee, J. X., Cuevas, B., Rastani, A., Elum, J. E., & Zweifel, L. S. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.918839 · Cited by 25 · see citing works
Forebrain-Midbrain Circuits and Peptides Involved in Hyperalgesia After Chronic Alcohol Exposure
Gilpin, N. W. (2021) · Alcohol research · doi:10.35946/arcr.v41.1.13 · Cited by 14 · see citing works
Bertagna, N. B., Wilson, L., Bailey, C. K., Cruz, F. C., Albrechet‐Souza, L., & Wills, T. A. (2023) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.15228 · Cited by 13 · see citing works
CRF regulates pain sensation by enhancement of corticoaccumbal excitatory synaptic transmission
Zhao, W.-N., Yu, Y., Wang, X., Xia, S.-H., Ma, Y., Tang, H., Tao, M., Li, H., Xu, Z., Yang, J., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02488-7 · Cited by 13 · see citing works
Mindaye, S. A., Chen, W.-H., Lin, S.-C., Chen, Y.-C., Abdelaziz, M. A., Tzeng, Y.-S., Shih, A. C.-C., Chen, S.-Y., Yang, S., & Chen, C. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114946 · Cited by 13 · see citing works
Sex differences in BNST signaling and BNST CRF in fear processingPreprint
Hon, O. J., Neira, S., Flanigan, M. E., Roland, A. V., Caira, C. M., Sides, T. R., D'Ambrosio, S. L., Lee, S., Simpson, Y., Buccini, M. C., et al. (2023) · eLife · doi:10.7554/elife.89189 · Cited by 10 · see citing works
Self-citationGyawali, U., Martin, D. A., Sun, F., Li, Y., & Calu, D. J. (2023) · eLife · doi:10.7554/elife.81980 · Cited by 9 · see citing works
Gianessi, C. A., Haun, H. L., Pati, D., Sides, T. R., D’Ambrosio, S., Kelson, W. P., Hernandez, R., Gereau, G. B., Boyt, K. M., Hodge, C. W., et al. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02192-2 · Cited by 11 · see citing works
Self-citationBertagna, N. B., Holmgren, E. B., Engi, S. A., Ha, L., Cruz, F. C., Albrechet‐Souza, L., & Wills, T. A. (2024) · Psychopharmacology · doi:10.1007/s00213-024-06693-8 · Cited by 7 · see citing works
Neuromodulatory signaling contributing to the encoding of aversion
Wu, C.-H., Camelot, L., Lecca, S., & Mameli, M. (2025) · Trends in Neurosciences · doi:10.1016/j.tins.2025.04.003 · Cited by 5 · see citing works
Hagiwara, H., Sakimura, K., Abe, M., Itoi, K., Kamiya, Y., Akema, T., & Funabashi, T. (2021) · Brain Research · doi:10.1016/j.brainres.2021.147688 · Cited by 5 · see citing works
Dopamine D2 receptors in the bed nucleus of the stria terminalis modulate alcohol-related behaviors
Pati, D., Taxier, L. R., Xia, M., Lee, S. I., Conley, S. Y., Sides, T. R., Boyt, K. M., Hunker, A. C., Zweifel, L. S., & Kash, T. L. (2024) · Addiction Neuroscience · doi:10.1016/j.addicn.2024.100157 · Cited by 4 · see citing works
Self-citationKanaya, M., Ueta, Y., Mochizuki‐Kashio, M., Nakamura‐Ishizu, A., & Miyata, M. (2025) · Frontiers in Neural Circuits · doi:10.3389/fncir.2025.1593443 · Cited by 3 · see citing works
A brainstem pathway underlying vagal modulation of somatic pain and affective states
Tang, Y., Shao, R., Luo, L., Liao, L., Wang, X., Zhu, H., Xiao, X., & Deng, H. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02313-0 · Cited by 3 · see citing works
The bed nucleus of the stria terminalis in threat detection: task choice and rodent experience
Sherman, E. R., Thomas, J. J., & Cahill, E. (2022) · Emerging Topics in Life Sciences · doi:10.1042/etls20220002 · Cited by 3 · see citing works
Sex differences in BNST signaling and BNST CRF in fear processing
Hon, O. J., Neira, S., Flanigan, M. E., Roland, A. V., Caira, C. M., Sides, T. R., D’Ambrosio, S., Lee, S., Simpson, Y., Buccini, M. C., et al. (2025) · eLife · doi:10.1101/2023.04.10.535848 · Cited by 2 · see citing works
Self-citationA Mechanistic Model for the HPA Axis Cortisol Paradox in PTSDPreprint
Danan, D., Grosskopf, Y., Hayut, Y., Toledano, Y., Doenyas‐Barak, K., Mayo, A., & Alon, U. S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.13.681561 · Cited by 1 · see citing works
Hon, O. J., Flanigan, M. E., Roland, A. V., Caira, C. M., Sides, T. R., D’Ambrosio, S., Lee, S., Simpson, Y., Buccini, M. C., Machinski, S. N., et al. (2023) · eLife · doi:10.7554/elife.89189.1 · Cited by 1 · see citing works
Self-citationHon, O. J., Neira, S., Flanigan, M. E., Roland, A. V., Caira, C. M., Sides, T. R., D’Ambrosio, S., Lee, S., Simpson, Y., Buccini, M. C., et al. (2025) · eLife · doi:10.7554/elife.89189.2
Self-citationSex Differences in Bed Nucleus of the Stria Terminalis Response to Calcitonin Gene-Related PeptidePreprint
Lorsung, R. M., Ji, Y., Cramer, N., Aitken, R., Han, S., Masri, R. M., & Keller, A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.21.726958
Romero, J. M., Stafford-Trujillo, S.-M., Mendoza, M., Chin, P.-S., Srivastava, S., Kochukov, M. Y., Tong, Q., & Arenkiel, B. R. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1876369
- Authors
- Yu, W., Caira, C. M., del R. Rivera Sanchez, N., Moseley, G. A., & Kash, T. L.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Kash, Thomas L.
- Venue
- Scientific Reports
- Published
- 2021-06-14
- Volume
- 11
- Issue
- 1
- Pages
- 12500-12500
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC8203647
- OpenAlex
- W3168280339
- Cited by
- 25
- References
- 91
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 5 · 2023: 5 · 2022: 3 · 2021: 3
- FWCI
- 2.51
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute on Alcohol Abuse and Alcoholism (F31AA027129, R21AA027460)
- National Institute of General Medical Sciences (T32GM007040)
- Topics
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- corticotropin-releasing factor, bed nucleus of the stria terminalis, pain processing, sex differences, nociception, thermal pain, CRF neurons, neuronal activity, pain behavior
- MeSH terms
- Animals, Corticotropin-Releasing Hormone, Disease Models, Animal, Female, Hot Temperature, Humans, Male, Mice, Transgenic, Neurons, Pain, Septal Nuclei, Sex Factors, Mice, Nociception, Optical Imaging
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
