Cited by 31Neuroendocrine regulation and behaviorSexual Differentiation and DisordersAnimal Behavior and Reproduction

The Effects of Neonatal Castration on the Subsequent Behavioural Response to Centrally Administered Arginine Vasopressin and the Expression of V1a Receptors in Adult Male Prairie Voles

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Cushing, B. S., Okorie, U., Young, L. J.·2003·Journal of Neuroendocrinology

Abstract

Centrally administered arginine vasopressin induces the formation of partner preferences in male prairie voles (Microtus ochrogaster). The expression of many vasopressin‐regulated behaviours is testosterone dependent. In this study, we tested the hypothesis that early exposure to gonadal steroids are necessary to establish the typical response of adult male prairie voles to exogenous vasopressin, predicting that adult males which were castrated neonatally would not form partner preferences in response to centrally administered vasopressin. We also examined the effect of neonatal castration on the expression of vasopressin (V 1a) receptors. Voles were castrated on the day of birth (NEOCAST), sham‐castrated on the day of birth (NEOSHAM) or castrated as adults (ADULTCAST). With the exception of one group of neonatal sham males (NEOSHAM CON), which served as a control for the effects of vasopressin, as adults, all males received a 1‐µl intracerebroventricular injection of vasopressin (100 ng) in artificial cerebrospinal fluid. In addition, 2 weeks before testing, one group of neonatally castrated males received an implant of testosterone propionate (NEOCAST + TP). Between 60 and 90 days of age, an internal cannula was placed in the lateral cerebral ventricle and, 24 h later, males were injected with vasopressin. Subsequently, after an additional 15 min, males were cohabitated with a female ‘partner’ for 1 h. Immediately following cohabitation, males were placed in a Y‐shaped partner preference test apparatus for 3 h, in which the male had access to the ‘partner’ and a novel female, ‘stranger.’ Time spent with the partner versus the stranger was compared within and between treatments. The results were found to support our hypothesis as the NEOSHAM and ADULTCAST males formed partner preferences, spending more time with the partner, and they spent significantly more time with their partner than did NEOSHAM CON, NEOCAST or NEOCAST + TP males. Replacement of testosterone in neonatally castrated males did not restore partner preference formation in response to vasopressin in adult males. Finally, neonatal castration did not affect the distribution of V 1a receptors.

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Crossref · 10.1046/j.1365-2826.2003.01097.x

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  • Because AVP/OT and the dopaminergic pathways they feed into are heavily influenced by sex steroids across the lifespan, their sexually dimorphic ontogeny and function may be particularly vulnerable to endocrine disruption.

    “Because AVP/OT and the dopaminergic pathways they feed into are heavily influenced by sex steroids across the lifespan (50–59), it is highly plausible that their sexually dimorphic ontogeny and function may be particularly vulnerable to endocrine disruption.”

    From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [52]

    The Discussion reports that early removal of gonadal steroids changes adult male prairie voles’ behavioral response to vasopressin, and the Abstract says steroids maintain the vasopressin system in adult males. This supports steroid influence on AVP across developmental stages, but the paper does not establish the same claim for oxytocin or dopaminergic pathways. The endocrine-disruption inference follows the citation and is the citing authors’ own framing. (LLM, conf=0.86)

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  • Males gonadectomized on the day of birth fail to form a pair bond after AVP administration.

    “Males gonadectomized on the day of birth, for example, fail to form a pair bond after AVP administration (52).”

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Research works printed but not linked: 3

  1. Insel TR, Young LJ. Neurobiology of social attachment. Nature Neurosci Rev 2001; 2: 129±136.
  2. Kirkpatrick B, Carter CS, Newman SW, Insel TR. Axon-sparing lesions of the medial nucleus of the amygdala decrease af®liative behaviors in the prairie vole (Microtus ochrogaster). Behav Neurosci 1994; 108: 501±513.
  3. Young LJ, Toloczko D, Insel TR. Localization of vasopressin (V1a) receptor binding and mRNA in Rhesus monkey brain. J Neuroendocrinol 1999; 11: 291.

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Authors
Cushing, B. S., Okorie, U., & Young, L. J.
Affiliations
  • University of Illinois Chicago (US)
  • University of Maryland, College Park (US)
  • Emory University (US)
Corresponding author
Cushing, B. S.
Venue
Journal of Neuroendocrinology
Publisher
Wiley
Published
2003-10-21
Volume
15
Issue
11
Pages
1021-1026
ISSN
  • 0953-8194 (ISSN-L)
  • 1365-2826
OpenAlex
W1525996370
Cited by
31
References
53
Citations by year
2025: 3 · 2022: 2 · 2018: 1 · 2017: 3 · 2016: 2 · 2014: 2 · 2013: 1 · 2012: 1
FWCI
1.39
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroendocrinology (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation (9876754)
  • National Institutes of Health
  • National Institute of Mental Health (MH 01992, K01MH001992)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD038490, HD38490)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
neonatal castration, vasopressin, V1a receptor, mate preferences, Microtus ochrogaster, testosterone, intracerebroventricular administration, social behavior
MeSH terms
Age Factors, Animals, Animals, Newborn, Arginine Vasopressin, Brain, Castration, Choice Behavior, Arvicolinae, Male, Sexual Behavior, Animal, Testosterone, Receptors, Vasopressin, Recognition, Psychology

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