• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Jul 1, 1992; 89(13): 5981–5985.
PMCID: PMC402122

Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles.

Abstract

The neuropeptide oxytocin has been implicated in the mediation of several forms of affiliative behavior including parental care, grooming, and sex behavior. Here we demonstrate that species from the genus Microtus (voles) selected for differences in social affiliation show contrasting patterns of oxytocin receptor expression in brain. By in vitro receptor autoradiography with an iodinated oxytocin analogue, specific binding to brain oxytocin receptors was observed in both the monogamous prairie vole (Microtus ochrogaster) and the polygamous montane vole (Microtus montanus). In the prairie vole, oxytocin receptor density was highest in the prelimbic cortex, bed nucleus of the stria terminalis, nucleus accumbens, midline nuclei of the thalamus, and the lateral aspects of the amygdala. These brain areas showed little binding in the montane vole, in which oxytocin receptors were localized to the lateral septum, ventromedial nucleus of the hypothalamus, and cortical nucleus of the amygdala. Similar differences in brain oxytocin receptor distribution were observed in two additional species, the monogamous pine vole (Microtus pinetorum) and the polygamous meadow vole (Microtus pennsylvanicus). Receptor distributions for two other neurotransmitter systems implicated in the mediation of social behavior, benzodiazepines, and mu opioids did not show comparable species differences. Furthermore, in the montane vole, which shows little affiliative behavior except during the postpartum period, brain oxytocin receptor distribution changed within 24 hr of parturition, concurrent with the onset of maternal behavior. We suggest that variable expression of the oxytocin receptor in brain may be an important mechanism in evolution of species-typical differences in social bonding and affiliative behavior.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.5M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Shapiro LE, Dewsbury DA. Differences in affiliative behavior, pair bonding, and vaginal cytology in two species of vole (Microtus ochrogaster and M. montanus). J Comp Psychol. 1990 Sep;104(3):268–274. [PubMed]
  • Shapiro LE, Insel TR. Infant's response to social separation reflects adult differences in affiliative behavior: a comparative developmental study in prairie and montane voles. Dev Psychobiol. 1990 Jul;23(5):375–393. [PubMed]
  • Keverne EB, Martensz ND, Tuite B. Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology. 1989;14(1-2):155–161. [PubMed]
  • Panksepp J, Herman B, Conner R, Bishop P, Scott JP. The biology of social attachments: opiates alleviate separation distress. Biol Psychiatry. 1978 Oct;13(5):607–618. [PubMed]
  • Hansen S, Ferreira A, Selart ME. Behavioural similarities between mother rats and benzodiazepine-treated non-maternal animals. Psychopharmacology (Berl) 1985;86(3):344–347. [PubMed]
  • Insel TR, Hill JL, Mayor RB. Rat pup ultrasonic isolation calls: possible mediation by the benzodiazepine receptor complex. Pharmacol Biochem Behav. 1986 May;24(5):1263–1267. [PubMed]
  • Insel TR. Oxytocin--a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology. 1992;17(1):3–35. [PubMed]
  • Unnerstall JR, Niehoff DL, Kuhar MJ, Palacios JM. Quantitative receptor autoradiography using [3H]ultrofilm: application to multiple benzodiazepine receptors. J Neurosci Methods. 1982 Jul;6(1-2):59–73. [PubMed]
  • Insel TR, Kinsley CH, Mann PE, Bridges RS. Prenatal stress has long-term effects on brain opiate receptors. Brain Res. 1990 Mar 12;511(1):93–97. [PubMed]
  • Elands J, Barberis C, Jard S, Tribollet E, Dreifuss JJ, Bankowski K, Manning M, Sawyer WH. 125I-labelled d(CH2)5[Tyr(Me)2,Thr4,Tyr-NH2(9)]OVT: a selective oxytocin receptor ligand. Eur J Pharmacol. 1988 Mar 1;147(2):197–207. [PubMed]
  • Shapiro LE, Insel TR. Ontogeny of oxytocin receptors in rat forebrain: a quantitative study. Synapse. 1989;4(3):259–266. [PubMed]
  • Tribollet E, Barberis C, Jard S, Dubois-Dauphin M, Dreifuss JJ. Localization and pharmacological characterization of high affinity binding sites for vasopressin and oxytocin in the rat brain by light microscopic autoradiography. Brain Res. 1988 Feb 23;442(1):105–118. [PubMed]
  • Pedersen CA, Prange AJ., Jr Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6661–6665. [PMC free article] [PubMed]
  • Fahrbach SE, Morrell JI, Pfaff DW. Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm Behav. 1984 Sep;18(3):267–286. [PubMed]
  • Kendrick KM, Keverne EB, Baldwin BA. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology. 1987 Jun;46(1):56–61. [PubMed]
  • Arletti R, Bertolini A. Oxytocin stimulates lordosis behavior in female rats. Neuropeptides. 1985 Jun;6(3):247–253. [PubMed]
  • Caldwell JD, Prange AJ, Jr, Pedersen CA. Oxytocin facilitates the sexual receptivity of estrogen-treated female rats. Neuropeptides. 1986 Feb-Mar;7(2):175–189. [PubMed]
  • Insel TR, Winslow JT. Central administration of oxytocin modulates the infant rat's response to social isolation. Eur J Pharmacol. 1991 Oct 2;203(1):149–152. [PubMed]
  • Fahrbach SE, Morrell JI, Pfaff DW. Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology. 1985 Jun;40(6):526–532. [PubMed]
  • Insel TR, Harbaugh CR. Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol Behav. 1989 May;45(5):1033–1041. [PubMed]
  • Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ., Jr Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides. 1985 Apr;6(2):175–182. [PubMed]
  • Witt DM, Insel TR. A selective oxytocin antagonist attenuates progesterone facilitation of female sexual behavior. Endocrinology. 1991 Jun;128(6):3269–3276. [PubMed]
  • Pfaff D, Keiner M. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol. 1973 Sep 15;151(2):121–158. [PubMed]
  • Insel TR. Postpartum increases in brain oxytocin binding. Neuroendocrinology. 1986;44(4):515–518. [PubMed]
  • Carter CS, Witt DM, Schneider J, Harris ZL, Volkening D. Male stimuli are necessary for female sexual behavior and uterine growth in prairie voles (Microtus ochrogaster). Horm Behav. 1987 Mar;21(1):74–82. [PubMed]
  • Caldwell JD, Jirikowski GF, Greer ER, Stumpf WE, Pedersen CA. Ovarian steroids and sexual interaction alter oxytocinergic content and distribution in the basal forebrain. Brain Res. 1988 Apr 19;446(2):236–244. [PubMed]
  • Kendrick KM, Keverne EB, Chapman C, Baldwin BA. Microdialysis measurement of oxytocin, aspartate, gamma-aminobutyric acid and glutamate release from the olfactory bulb of the sheep during vaginocervical stimulation. Brain Res. 1988 Feb 23;442(1):171–174. [PubMed]
  • Witt DM, Carter CS, Walton DM. Central and peripheral effects of oxytocin administration in prairie voles (Microtus ochrogaster). Pharmacol Biochem Behav. 1990 Sep;37(1):63–69. [PubMed]
  • LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM. The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci. 1990 Apr;10(4):1062–1069. [PubMed]
  • Everitt BJ, Cador M, Robbins TW. Interactions between the amygdala and ventral striatum in stimulus-reward associations: studies using a second-order schedule of sexual reinforcement. Neuroscience. 1989;30(1):63–75. [PubMed]
  • Phillips AG. Brain reward circuitry: a case for separate systems. Brain Res Bull. 1984 Feb;12(2):195–201. [PubMed]
  • Gray JA, McNaughton N. Comparison between the behavioural effects of septal and hippocampal lesions: a review. Neurosci Biobehav Rev. 1983 Summer;7(2):119–188. [PubMed]
  • Fleischer S, Slotnick BM. Disruption of maternal behavior in rats with lesions of the septal area. Physiol Behav. 1978 Aug;21(2):189–200. [PubMed]
  • Kondo Y, Shinoda A, Yamanouchi K, Arai Y. Role of septum and preoptic area in regulating masculine and feminine sexual behavior in male rats. Horm Behav. 1990 Sep;24(3):421–434. [PubMed]
  • Insel TR, Gelhard R, Shapiro LE. The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice. Neuroscience. 1991;43(2-3):623–630. [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...