Literature DB >> 34189787

Compositional variation in early-life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster).

Forrest D Rogers1,2, Sara M Freeman2,3,4, Marina Anderson2,3, Michelle C Palumbo2,3,5, Karen L Bales2,3.   

Abstract

Paternal absence can significantly alter bio-behavioural development in many biparental species. This effect has generally been demonstrated by comparing the development of offspring reared under biparental care with those reared by a single mother. However, studies employing this design conflate two significant modifications to early-life experience: removal of father-specific qualities and the general reduction of offspring-directed care. In the socially monogamous prairie vole (Microtus ochrogaster), the experience of paternal absence without substitution during development inhibits partner preference formation in adulthood, a hallmark of social monogamy, in females and males. Employing alloparents as substitutes for fathers, our previous work demonstrated that paternal absence affects pair-bond formation in female offspring via reduced quantity of care, although it affects pair-bond formation in male offspring by means of a missing paternal quality (or qualities). Here, we present evidence that paternal absence (with and without alloparental substitution) may alter the ontogeny of neural oxytocin receptor (OXTR) and/or vasopressin 1a receptor (AVPR1a) distribution in male and female prairie voles. Compared to biparentally reared controls (BPC), male offspring reared in mother only (MON) and maternal-plus-alloparental (MPA) conditions show lower densities of OXTR in the central amygdala; and MPA males show lower densities of OXTR in the caudate putamen and nucleus accumbens. Early-life experience was not associated with differences in AVPR1a density in males. However, MON and MPA females show greater densities of AVPR1a in the medial amygdala than BPC; and MPA females show greater densities of AVPR1a in the ventromedial nucleus of the hypothalamus. We also demonstrate with corticosterone concentrations that MON and MPA offspring are not differentially susceptible to a stressor (ie, social isolation) than BPC offspring. These findings suggest that paternal absence, although likely not a salient early-life stressor, has neuroendocrine consequences for offspring, some of which may affect partner preference formation.
© 2021 British Society for Neuroendocrinology.

Entities:  

Keywords:  fathers; oxytocin; parenting; paternal deprivation; vasopressin

Mesh:

Substances:

Year:  2021        PMID: 34189787      PMCID: PMC8486352          DOI: 10.1111/jne.13001

Source DB:  PubMed          Journal:  J Neuroendocrinol        ISSN: 0953-8194            Impact factor:   3.870


  49 in total

Review 1.  The neurobiology of pair bonding.

Authors:  Larry J Young; Zuoxin Wang
Journal:  Nat Neurosci       Date:  2004-10       Impact factor: 24.884

2.  Paternal deprivation alters region- and age-specific interneuron expression patterns in the biparental rodent, Octodon degus.

Authors:  Katharina Braun; Katja Seidel; Solveig Weigel; Christian Roski; Gerd Poeggel
Journal:  Cereb Cortex       Date:  2010-12-02       Impact factor: 5.357

3.  Social modulation of corticosteroid responses in male prairie voles.

Authors:  A C DeVries; S E Taymans; C S Carter
Journal:  Ann N Y Acad Sci       Date:  1997-01-15       Impact factor: 5.691

4.  Early rearing experience is related to altered aggression and vasopressin production following chronic social isolation in the prairie vole.

Authors:  Allison M Perkeybile; Karen L Bales
Journal:  Behav Brain Res       Date:  2015-01-24       Impact factor: 3.332

5.  Distributions of oxytocin and vasopressin 1a receptors in the Taiwan vole and their role in social monogamy.

Authors:  A R Chappell; S M Freeman; Y K Lin; J L LaPrairie; K Inoue; L J Young; L D Hayes
Journal:  J Zool (1987)       Date:  2016-03-01       Impact factor: 2.322

6.  Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles.

Authors:  Rui Jia; Fadao Tai; Shucheng An; Xia Zhang; Hugh Broders
Journal:  Behav Processes       Date:  2009-07-25       Impact factor: 1.777

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

Authors:  T R Insel; L E Shapiro
Journal:  Proc Natl Acad Sci U S A       Date:  1992-07-01       Impact factor: 11.205

8.  Cooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation.

Authors: 
Journal:  Anim Behav       Date:  1998-05       Impact factor: 2.844

9.  Early life stress alters transcriptomic patterning across reward circuitry in male and female mice.

Authors:  Catherine Jensen Peña; Milo Smith; Aarthi Ramakrishnan; Hannah M Cates; Rosemary C Bagot; Hope G Kronman; Bhakti Patel; Austin B Chang; Immanuel Purushothaman; Joel Dudley; Hirofumi Morishita; Li Shen; Eric J Nestler
Journal:  Nat Commun       Date:  2019-11-08       Impact factor: 14.919

10.  Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster).

Authors:  Allison M Perkeybile; Luana L Griffin; Karen L Bales
Journal:  Front Behav Neurosci       Date:  2013-03-18       Impact factor: 3.558

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  5 in total

1.  Individual and Combined Effects of Paternal Deprivation and Developmental Exposure to Firemaster 550 on Socio-Emotional Behavior in Prairie Voles.

Authors:  Sagi Enicole A Gillera; William P Marinello; Mason A Nelson; Brian M Horman; Heather B Patisaul
Journal:  Toxics       Date:  2022-05-22

Review 2.  The oxytocin system and early-life experience-dependent plastic changes.

Authors:  Tatsushi Onaka; Yuki Takayanagi
Journal:  J Neuroendocrinol       Date:  2021-10-29       Impact factor: 3.870

Review 3.  The neural circuits of monogamous behavior.

Authors:  María Fernanda López-Gutiérrez; Sara Mejía-Chávez; Sarael Alcauter; Wendy Portillo
Journal:  Front Neural Circuits       Date:  2022-09-29       Impact factor: 3.342

4.  Transcriptomic analysis of paternal behaviors in prairie voles.

Authors:  Florian Duclot; Yan Liu; Samantha K Saland; Zuoxin Wang; Mohamed Kabbaj
Journal:  BMC Genomics       Date:  2022-10-01       Impact factor: 4.547

5.  Emergent intra-pair sex differences and organized behavior in pair bonded prairie voles (Microtus ochrogaster).

Authors:  Liza E Brusman; David S W Protter; Allison C Fultz; Maya U Paulson; Gabriel D Chapel; Isaiah O Elges; Ryan T Cameron; Annaliese K Beery; Zoe R Donaldson
Journal:  Genes Brain Behav       Date:  2022-01-19       Impact factor: 3.449

  5 in total

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