Species and sex differences in brain distribution of corticotropin‐releasing factor receptor subtypes 1 and 2 in monogamous and promiscuous vole species
Abstract
Corticotropin‐releasing factor (CRF) receptor subtypes 1 and 2 have been implicated in rodent models of anxiety, but much less is known about the CRF system and social behavior. Both corticosterone and central CRF receptors modulate pair bonding in the monogamous prairie vole. Using receptor autoradiography, we mapped CRFR 1 and CRFR 2 in the brains of two monogamous vole species, the prairie vole and pine vole, and two promiscuous vole species, the meadow vole and montane vole. We found markedly different patterns of brain CRFR 1 and CRFR 2 binding among the four species, including species differences in the olfactory bulb, nucleus accumbens, lateral septum, hippocampus, laterodorsal thalamus, cingulate cortex, superior colliculus, and dorsal raphe. Interestingly, we also observed striking sex differences in voles: CRFR 2 binding was higher in the encapsulated bed nucleus of the stria terminalis in males than females for all four vole species. These results suggest possible sites of action for CRF‐induced facilitation of pair bond formation in prairie voles, as well as potential sex differences in the CRF modulation of pair bonding. Further examination of CRF receptors in vole species may reveal a novel role for CRF in social behavior. Ultimately, our results identify several brain regions with conserved CRF receptor patterns across rodent and primate species, in contrast to several brain regions with phylogenetically plastic CRF receptor patterns, and have interesting implications for the evolution of CRF receptor patterns and behavior. J. Comp. Neurol. 487:75–92, 2005. © 2005 Wiley‐Liss, Inc.
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Monogamous and non-monogamous vole species differ greatly in brain distribution of CRF-R1 and CRF-R2, while CRF peptide distribution is highly conserved.
“Monogamous and non-monogamous species of voles differ greatly in the distribution of CRF-R1 and CRF-R2 in the brain, even while the distribution of CRF peptide is highly conserved (Lim et al 2005; Lim et al 2006).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Lim et al 2005
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A Neuroscientist’s Guide to the Vole
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“…in the brains of monogamous (pine and prairie) vole species compared to promiscuous (montane and meadow) vole species (Insel & Shapiro, 1992; Lim et al., 2005; Smeltzer et al., 2006; described in detail above) or on genetic differences in sequences regulating expression of the arginine…”
Schulkin, J. A. (2011) · Brain Research · doi:10.1016/j.brainres.2011.03.055 · Cited by 51 · see citing works
“This region contains both glucocorticoids and CRH receptors (e.g., Lim et al., 2005).”
BackgroundVuppaladhadiam, L., Ehsan, C., Akkati, M., & Bhargava, A. (2020) · Cells · doi:10.3390/cells9040839 · Cited by 50 · see citing works
Distribution of Corticotropin-Releasing Factor and Urocortin 1 in the Vole Brain
Lim, M. M., Tsivkovskaia, N. O., Bai, Y., Young, L. J., & Ryabinin, A. E. (2006) · Brain, Behavior and Evolution · doi:10.1159/000094360 · Cited by 48 · see citing works
“This protocol has been successfully Lim /Tsivkovskaia /Bai /Young /Ryabinin Brain Behav Evol 2006;68:229–240 232 employed in vole brains [Lim et al., 2005].”
InfluentialSelf-citationNorthcutt, K. V., Wang, Z., & Lonstein, J. S. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21148 · Cited by 46 · see citing works
“…species differ in numerous ways, including expression of receptors for oxytocin (Insel and Shapiro, 1992), vasopressin (Insel et al., 1994), corticotropin-releasing factor (Lim et al., 2005), estrogen (Fowler et al., 2005), and dopamine (Curtis, Fowler, Lon- stein, and Wang, in preparation).”
BackgroundWeathington, J. M., & Cooke, B. M. (2012) · Endocrinology · doi:10.1210/en.2012-1815 · Cited by 45 · see citing works
High variability and non-neutral evolution of the mammalian avpr1a gene
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“oxytocin, see in [16,20,70]; serotonin, see in [71,72]; corticothropin, see in [73, 74 ]).”
BackgroundSchulkin, J. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.4/jschulkin · Cited by 49 · see citing works
Central release of oxytocin and the ventromedial hypothalamus
Sabatier, N., Rowe, I. C. M., & Leng, G. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351247 · Cited by 40 · see citing works
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“Using the total and CRF2 binding values, CRF1 binding was calculated as total 125I-sauvagine binding minus CRF2 binding (Sanchez et al., 1999; Lim et al., 2005).”
BackgroundMethodSelf-citationWeiser, M. J., Goel, N., Sandau, U. S., Bale, T. L., & Handa, R. J. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.07.013 · Cited by 35 · see citing works
“Furthermore, in the male vole, CRHR2 binding is higher in the bed nucleus of the stria terminalis (BST) than in the female vole (Lim et al., 2005).”
BackgroundHostetler, C. M., Hitchcock, L. N., Anacker, A. M. J., Young, L. J., & Ryabinin, A. E. (2012) · Peptides · doi:10.1016/j.peptides.2012.12.008 · Cited by 34 · see citing works
“For example, Microtus species show species differences that reflect social organization in a number of peptide systems including arginine vasopressin (V1a receptor: [33,37]), oxytocin (OT receptor: [32,37], corticotrophin releasing factor (CRF, urocortin 1, and receptor subtypes 1 and 2: [38,39] and CART peptide [28].”
BackgroundSelf-citationRosinger, Z. J., Jacobskind, J. S., Guzman, R. M. D., Justice, N. J., & Zuloaga, D. G. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.04.045 · Cited by 34 · see citing works
“In voles, a sex difference in CRFR2 has been found in the bed nucleus of the stria terminalis (males > females; Lim et al., 2005).”
BackgroundKlampfl, 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
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“Consistent with hese findings, and consistent with expression of functional eceptor protein in the DR, dense CRF2 receptor binding has been described in the DR of several vole species (Lim et al., 2005).”
Corticotropin-releasing factor receptor densities vary with photoperiod and sociality
Beery, A. K., Vahaba, D. M., & Grunberg, D. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.08.014 · Cited by 30 · see citing works
“Across four species of voles, monogamous species had lower CRF1 receptor density in the nucleus accumbens than promiscuous species (Lim et al., 2005).”
BackgroundMethodInfluentialInoue, K., Burkett, J. P., & Young, L. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.035 · Cited by 31 · see citing works
“P A A uthor M anuscript behavior between prairie and meadow voles (Lim et al., 2004, Lim et al., 2005b, Lim et al., 2007, Ross et al., 2009).”
BackgroundMethodSelf-citationSeasonal Variation in Group Size Is Related to Seasonal Variation in Neuropeptide Receptor Density
Wilson, L. C., Goodson, J. L., & Kingsbury, M. A. (2016) · Brain Behavior and Evolution · doi:10.1159/000448372 · Cited by 30 · see citing works
“The 125 I-SG binding that we observed indicated that putative CHR receptors in both seasonally flocking and nonflocking sparrows show a similar pattern to that reported in mammals [Van Pett et al., 2000; Lim et al., 2005], with binding sites distributed throughout the forebrain.”
ResultDrinking alcohol has sex-dependent effects on pair bond formation in prairie voles
Anacker, A. M. J., Ahern, T. H., Hostetler, C. M., Dufour, B. D., Smith, M. L., Cocking, D. L., Li, J., Young, L. J., Loftis, J. M., & Ryabinin, A. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320879111 · Cited by 29 · see citing works
“This region is of particular interest because there is a sex-dependent difference in the number of CRF2 receptors in the BNST, with male prairie voles having greater receptor binding than females (53).”
BackgroundSelf-citationRosinger, Z. J., Jacobskind, J. S., Park, S. G., Justice, N. J., & Zuloaga, D. G. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.08.016 · Cited by 29 · see citing works
“In voles, there are also reports of a sex difference in which males have significantly increased CRFR2 binding compared to females (Lim et al., 2005).”
BackgroundVecchiarelli, H. A., Morena, M., Lee, T. T. ‐., Nastase, A. S., Aukema, R. J., Leitl, K. D., Gray, J. M., Petrie, G. N., Tellez-Monnery, K., & Hill, M. N. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100470 · Cited by 26 · see citing works
“There are differences in CRH levels and CRH receptor type 1 (CRH-R1) expression and binding between males and females in regions we examined (Bangasser, 2013; Bangasser and Wiersielis, 2018), including in the amygdala (Lim et al., 2005; Weathington and Cooke, 2012) and prefrontal cortex (Daiwile et al.”
BackgroundMolecular Signaling and Translational Significance of the Corticotropin Releasing Factor System
Ronan, P. J., & Summers, C. H. (2011) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-385506-0.00006-5 · Cited by 24 · see citing works
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“In prairie voles, males have significantly higher CRFR2 binding in the BNST than females, and this sex difference is not found in promiscuous rats, mice, or nonhuman primates (Lim et al., 2005).”
BackgroundFluoxetine inhibits corticotropin-releasing factor (CRF)-induced behavioural responses in rats
Lowry, C. A., Lowry, C. A., Hale, M. W., Lowry, C. A., Hale, M. W., Plant, A., Windle, R. J., Lowry, C. A., Hale, M. W., Plant, A., et al. (2008) · Stress · doi:10.1080/10253890802309861 · Cited by 24 · see citing works
“1997, 2003), (2) the presence of both CRF type 1 (CRF1) receptor and CRF type 2 (CRF2) receptor binding, receptor mRNA expression or receptor immunoreactivity in the midbrain raphé nuclei (De Souza et al. 1985; Chalmers et al. 1995; Bittencourt and Sawchenko 2000; Chen et al. 2000; Pett et al. 2000; Day et al. 2004; L…”
BackgroundAVPR1A variation is linked to gray matter covariation in the social brain network of chimpanzees
Mulholland, M. M., Navabpour, S., Mareno, M. C., Schapiro, S. J., Young, L. J., & Hopkins, W. D. (2020) · Genes Brain & Behavior · doi:10.1111/gbb.12631 · Cited by 23 · see citing works
Self-citationFrom endophenotypes to evolution: social attachment, sexual fidelity and the avpr1a locus
Phelps, S. M. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.09.002 · Cited by 23 · see citing works
“In general, increasing overlap with male home-ranges also increases overlap with female home-ranges [12], but reduces effectiveness of mate guarding.”
BackgroundLocci, A., Yan, Y., Rodríguez, G., & Dong, H. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15157 · Cited by 21 · see citing works
Coen, C. W., Κalamatianos, T., Oosthuizen, M. K., Poorun, R., Faulkes, C. G., & Bennett, N. C. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23796 · Cited by 21 · see citing works
“…of CRF1 binding in the cingulate cortex and other neocortical fields are equivalent (moderate or high) in monogamous prairie and promiscuous meadow species but significantly greater in the promiscuous montane species (low or moderate) than in the monogamous pine species (weak; Lim et al., 2005).”
BackgroundMethodResultInfluentialHunter, R. G., Lim, M. M., Philpot, K. B., Young, L. J., & Kuhar, M. J. (2005) · Brain Research · doi:10.1016/j.brainres.2005.04.032 · Cited by 21 · see citing works
“In all the neuropeptides examined (V1aR, oxytocin receptor, CRF receptors 1 and 2), the neuropeptides themselves tend to be highly conserved between species, whereas receptor distribution is highly plastic and variable between species [22,23,35,48].”
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“Nucleus accumbens contains levels of corticotropin—releasing factor (CRF) receptors that are comparable to those in the amygdala (Aguilera et al., 2004; Lim et al., 2005).”
BackgroundSex, social status, and CRF receptor densities in naked mole‐rats
Beery, A. K., Bicks, L. K., Mooney, S. J., Goodwin, N. L., & Holmes, M. M. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23834 · Cited by 18 · see citing works
“CRF2 receptor binding in the habenula of naked mole-rats was notable; in prairie voles, meadow voles, and mice, CRF1 receptors are expressed in this region, with low to undetectable levels of CRF2 receptors (Chen et al., 2000; Lim et al., 2005; Beery et al., 2014).”
BackgroundResultInfluentialTan, L. A., Vaughan, J. M., Perrin, M. H., Rivier, J., & Sawchenko, P. E. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24307 · Cited by 17 · see citing works
Sex‐linked roles of the CRF 1 and the CRF 2 receptor in social behavior
Piccin, A., & Contarino, A. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24629 · Cited by 22 · see citing works
“Moreover, male voles showed higher CRF2 receptor binding sites than female voles in the bed nucleus of the stria terminalis, a brain region implicated in sex-linked social investigation (Chen & Hong, 2018; Lim et al., 2005).”
BackgroundCurtis, J. T., & Wang, Z. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.011 · Cited by 15 · see citing works
Comparative neurotranscriptomics reveal widespread species differences associated with bonding
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Urocortin II increases spontaneous parental behavior in prairie voles (Microtus ochrogaster)
SAMUEL, P., Hostetler, C. M., & Bales, K. L. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.08.015 · Cited by 14 · see citing works
“CRH2 receptors are found in many areas known to play a role in parental behavior, particularly the olfactory system and the periaqueductal grey [32;33].”
BackgroundThe Prairie Vole Model of Pair-Bonding and Its Sensitivity to Addictive Substances
Potretzke, S., & Ryabinin, A. E. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02477 · Cited by 15 · see citing works
Mate Selection, Sexual Orientation, and Pair Bonding
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The vasotocinergic system and its role in the regulation of stress in birds
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The effects of CRF and urocortins on the preference for social novelty of mice
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Comparative neurobiology and genetics of mammalian social behavior
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Medial amygdala ERα expression influences monogamous behaviour of male prairie voles in the field
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“(iii) The patterns of receptor expression for oxytocin [16], vasopressin [17], oestrogen [18], dopamine [19] and corticotrophin-releasing factor [20] vary predictably with reproductive strategies, degree of prosocial behaviour and aggression.”
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“, 1994), and in their corticotropin-releasing hormone (CRH) receptor expression in many areas of the brain (Lim et al., 2005).”
BackgroundThe role of dorsal raphe nucleus neuropeptides in reward and aversion
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“In particular, previous research indicates lower levels of CRFR1 binding the nucleus accumbens in socially monogamous (prairie and pine) voles versus promiscuous (meadow and montane voles) (Lim et al., 2005).”
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Corticotropin Releasing Factor Receptors and Agonistic Behavior in Syrian Hamsters
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Behavioral Alterations in Prairie Voles (Microtus ochrogaster) after Parent-Pup Separation
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Self-citation
- Authors
- Lim, M. M., Nair, H. P., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Lim, Miranda M.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2005-04-28
- Volume
- 487
- Issue
- 1
- Pages
- 75-92
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2053152793
- Cited by
- 95
- References
- 57
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 2 · 2021: 7 · 2020: 8 · 2019: 3 · 2018: 2 · 2017: 4 · 2016: 5 · 2015: 7 · 2014: 5 · 2013: 6 · 2012: 9
- FWCI
- 10.26
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH-64692, K02MH064692, F30MH065050, MH65050)
- National Center for Research Resources (RR-00 165, P51RR000165)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- corticotropin-releasing factor, CRF1 receptor, CRF receptor 2, brain receptor distribution, Microtus ochrogaster, pine vole, Microtus pennsylvanicus, montane vole, pair bonding, monogamy, promiscuity, sex differences, social behavior, corticosterone, bed nucleus of the stria terminalis
- MeSH terms
- CRF Receptor, Type 1, Analysis of Variance, Animals, Autoradiography, Brain, Brain Mapping, Arvicolinae, Female, Male, Neuronal Plasticity, Pair Bond, Sexual Behavior, Animal, Sex Characteristics, Social Behavior, Species Specificity, Tissue Distribution, Receptors, Corticotropin-Releasing Hormone, Statistics, Nonparametric
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