Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2017 Oct 11:8:265.
doi: 10.3389/fendo.2017.00265. eCollection 2017.

Vasopressinergic Neurocircuitry Regulating Social Attachment in a Monogamous Species

Maria C Tickerhoof  1 , Adam S Smith  1
Affiliations
Review

Vasopressinergic Neurocircuitry Regulating Social Attachment in a Monogamous Species

Maria C Tickerhoof et al. Front Endocrinol (Lausanne). .

Abstract

The prairie vole (Microtus ochrogaster) is a socially monogamous rodent species that forms a lasting connection between mates, known as a pair bond. The pair bond is primarily characterized by three distinct behaviors: partner preference, selective aggression, and biparental care of the young. The presence of these behaviors in the prairie vole and their absence in closely related non-monogamous species makes the prairie vole an important model of social relationships and facilitates the study of the neurobiological mechanisms of social affiliation and attachment. The nona-peptide arginine-vasopressin (AVP) is an important neuromodulator of social behavior and has been implicated in the regulation of the pair bond-related behaviors of the prairie vole, through activation of the AVP receptor subtype 1a (AVPR1a). Modulation of AVPR1a activity in different regions of the prairie vole brain impacts pair bond behavior, suggesting a role of AVP in neurocircuitry responsible for the regulation of social attachment. This review will discuss findings that have suggested the role of AVP in regulation of the pair bond-related behaviors of the prairie vole and the specific brain regions through which AVP acts to impact these unique behaviors.

Keywords: aggression; pair bond; parental care; partner preference; prairie vole; vasopressin.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Role of AVP in modulation of prairie vole partner preference. (A) A prairie vole breeding pair in direct side-by-side contact. Duration of this kind of contact is a typical marker for affiliation in a partner preference test. Photo credit: Charles Badland. (B) Male prairie voles have significantly greater AVP-ir fiber density in the LS compared with male meadow voles. *p < 0.05. Females of both species do not show robust AVP-ir fiber density in this region (data not shown). (C) Direct administration of AVPA into the LS of male prairie voles prior to a 24-h cohabitation with a sexually receptive female inhibits partner preference formation in a dose-dependent manner. *p < 0.01 versus duration in contact with the partner. (D) Direct infusion of AVP into the LS during a 6-h cohabitation with a non-receptive female induces partner preference in a dose-dependent manner. *p < 0.05 versus duration of contact with the partner. (E) Male prairie voles receiving a scrambled shRNA in the VP show a preference for the mate, but shRNA knockdown of AVPR1a in the VP leads to a preference for the stranger. *p < 0.05 between contact with the partner versus the stranger. (F) Administration of AVPA into the VP of male prairie voles inhibits partner preference formation. This effect is not seen in animals receiving Ringer’s solution, i.c.v. administration of AVPA, administration of AVPA into the medial amygdala or mediodorsal thalamus, or administration of a 10-fold lower dose of AVPA into the VP. *p < 0.05 versus duration of contact with the partner. (G) Meadow voles overexpressing AVPR1a in the VP show a preference for the partner over the stranger following 24-h cohabitation with a sexually receptive female. This effect is not seen in control animals or stereotactic misses. *p < 0.01 versus duration of contact with the stranger. AVP, arginine-vasopressin; AVPA, AVPR1a antagonist; AVPR1a, AVP receptor subtype 1a; i.c.v, intracerebroventricular; ir, immunoreactive; LS, lateral septum; VP, vasopressin. Adapted/reproduced from Wang (39) and Liu et al. (40) with permission from American Psychological Association, Barrett et al. (41) and Lim and Young (42) with permission from Elsevier, and Lim et al. (38) with permission from Nature Publishing Group.
Figure 2
Figure 2
Role of AVP in regulation of selective aggression in prairie voles. (A) Aggressive behavior is seen in prairie voles following cohabitation and mating with an opposite-sex animal. Photo credit: Charles Badland. (B) A significant increase in AVPR1a binding is observed in the AH of pair-bonded male prairie voles compared with sexually naïve male prairie voles. Scale bar is 1 mm. (C) Direct administration of AVP into the AH of sexually naïve male prairie voles induces aggressive behavior, and this effect is blocked by coadministration with AVPA. An increase in aggression is not observed with a stereotactic miss of the AH. Similarly, administration of AVPA into the AH of pair-bonded male prairie voles blocks bond-induced aggressive behavior. *p < 0.05 versus CSF-treated levels. (D) Virally mediated gene transfer of AVPR1a into the AH of sexually naïve male prairie voles induces aggressive behavior. *p < 0.05 versus LacZ vector control. AH, anterior hypothalamus; AVP, arginine-vasopressin; AVPA, AVPR1a antagonist; AVPR1a, AVP receptor subtype 1a; CSF, Cerebrospinal fluid. Adapted/reproduced from Gobrogge et al. (61) with permission from Proceedings of the National Academy of Sciences.
Figure 3
Figure 3
Impact of AVP activity in paternal behavior of prairie voles. (A) Prairie voles are a biparental species, and with the exception of nursing, fathers perform all of the same parental behaviors as mothers such as nest building, huddling, and grooming of the young. Photo credit: Charles Badland. (B) Prairie vole fathers show a significant decrease in AVP-ir fiber density in the LS relative to sexually naïve prairie voles. This effect is not seen in meadow voles. *p < 0.01 versus naïve voles. (C) Administration of AVP into the LS of sexually naïve prairie voles increases paternal responsiveness. *p < 0.0001 versus saline-treated animals. (D) Administration of 1 ng AVPA in the LS reduces the AVP-induced (0.1 ng AVP) increase in paternal responsiveness. *p < 0.05 versus saline/AVP-treated animals. (E) Administration of 1 ng AVPA reduces baseline levels of paternal responsiveness. *p < 0.001 versus saline-treated controls. AVP, arginine-vasopressin; AVPA, AVPR1a antagonist; LS, lateral septum. Adapted/reproduced from Bamshad et al. (51) with permission from Karger Publishers and Wang et al. (78) with permission from Proceedings of the National Academy of Sciences.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Kleiman DG. Monogamy in mammals. Q Rev Biol (1977) 52:39–69.10.1086/409721 - DOI - PubMed
    1. Getz LL, Carter CS, Gavish L. The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding. Behav Ecol Sociobiol (1981) 8:189–94.10.1007/BF00299829 - DOI
    1. Dewsbury DA. The comparative psychology of monogamy. Nebr Symp Motiv (1987) 35:1–50. - PubMed
    1. 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) 104:268–74.10.1037/0735-7036.104.3.268 - DOI - PubMed
    1. Gruder-Adams S, Getz LL. Comparison of the mating system and paternal behavior in Microtus ochrogaster and Microtus pennsylvanicus. J Mammal (1985) 66:165–7.10.2307/1380976 - DOI

LinkOut - more resources