Literature DB >> 17556547

Social control of brain morphology in a eusocial mammal.

Melissa M Holmes1, Greta J Rosen, Cynthia L Jordan, Geert J de Vries, Bruce D Goldman, Nancy G Forger.   

Abstract

Social status impacts reproductive behavior in diverse vertebrate species, but little is known about how it affects brain morphology. We explore this in the naked mole-rat, a species with the most rigidly organized reproductive hierarchy among mammals. Naked mole-rats live in large, subterranean colonies where breeding is restricted to a single female and small number of males. All other members of the colony, known as subordinates, are reproductively suppressed. Subordinates can become breeders if removed from the colony and placed with an opposite sex partner, but in nature most individuals never attain reproductive status. We examined the brains of breeding and subordinate naked mole-rats of both sexes, including several regions linked to reproduction and shown to be sexually dimorphic in other mammals. Stereological analyses revealed that neural morphology depends on status, such that breeders, regardless of sex, had more cells than subordinates in the ventromedial nucleus of the hypothalamus and a larger volume of the bed nucleus of the stria terminalis, paraventricular nucleus, and medial amygdala. Several other brain regions examined were unaffected. Surprisingly, males and females did not differ on any measure. These findings provide evidence that a change in social status triggers considerable neural remodeling and indicate that status, rather than sex, has a predominant role in determining neural structure in this remarkably social mammal.

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Year:  2007        PMID: 17556547      PMCID: PMC1965550          DOI: 10.1073/pnas.0610344104

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  46 in total

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Journal:  Proc Biol Sci       Date:  1996-12-22       Impact factor: 5.349

2.  Breeding status affects motoneuron number and muscle size in naked mole-rats: recruitment of perineal motoneurons?

Authors:  Marianne Seney; Bruce D Goldman; Nancy G Forger
Journal:  J Neurobiol       Date:  2006-10

3.  Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber.

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Journal:  J Reprod Fertil       Date:  1991-03

4.  Queen activation of lazy workers in colonies of the eusocial naked mole-rat.

Authors:  H K Reeve
Journal:  Nature       Date:  1992-07-09       Impact factor: 49.962

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Journal:  Proc Biol Sci       Date:  1997-07-22       Impact factor: 5.349

6.  Influence of gonadal sex hormones on behavioral components of the reproductive hierarchy in naked mole-rats.

Authors:  Sharry L Goldman; Nancy G Forger; Bruce D Goldman
Journal:  Horm Behav       Date:  2006-03-13       Impact factor: 3.587

7.  Social regulation of the electrical properties of gonadotropin-releasing hormone neurons in a cichlid fish (Astatotilapia burtoni).

Authors:  Anna K Greenwood; Russell D Fernald
Journal:  Biol Reprod       Date:  2004-05-12       Impact factor: 4.285

8.  Deletion of Bax eliminates sex differences in the mouse forebrain.

Authors:  Nancy G Forger; Greta J Rosen; Elizabeth M Waters; Dena Jacob; Richard B Simerly; Geert J de Vries
Journal:  Proc Natl Acad Sci U S A       Date:  2004-09-01       Impact factor: 11.205

9.  Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study.

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Journal:  J Comp Neurol       Date:  1990-04-01       Impact factor: 3.215

10.  Social regulation of gonadotropin-releasing hormone.

Authors:  Stephanie A White; Tuan Nguyen; Russell D Fernald
Journal:  J Exp Biol       Date:  2002-09       Impact factor: 3.312

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  20 in total

1.  Socially induced brain differentiation in a cooperatively breeding songbird.

Authors:  Cornelia Voigt; Stefan Leitner; Manfred Gahr
Journal:  Proc Biol Sci       Date:  2007-11-07       Impact factor: 5.349

2.  RFamide-related peptide-3 (RFRP-3) suppresses sexual maturation in a eusocial mammal.

Authors:  Diana E Peragine; Martha Pokarowski; Lucia Mendoza-Viveros; Ashlyn Swift-Gallant; Hai-Ying M Cheng; George E Bentley; Melissa M Holmes
Journal:  Proc Natl Acad Sci U S A       Date:  2017-01-17       Impact factor: 11.205

Review 3.  Stress in groups: Lessons from non-traditional rodent species and housing models.

Authors:  Annaliese K Beery; Melissa M Holmes; Won Lee; James P Curley
Journal:  Neurosci Biobehav Rev       Date:  2020-04-09       Impact factor: 8.989

4.  Social status and sex effects on neural morphology in Damaraland mole-rats, Fukomys damarensis.

Authors:  Jeff J Anyan; Marianne L Seney; Amanda Holley; Lynn Bengston; Bruce D Goldman; Nancy G Forger; Melissa M Holmes
Journal:  Brain Behav Evol       Date:  2011-06-24       Impact factor: 1.808

5.  Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain.

Authors:  Melissa M Holmes; Bruce D Goldman; Nancy G Forger
Journal:  Horm Behav       Date:  2008-03-28       Impact factor: 3.587

6.  Distribution of oxytocin in the brain of a eusocial rodent.

Authors:  G J Rosen; G J de Vries; S L Goldman; B D Goldman; N G Forger
Journal:  Neuroscience       Date:  2008-06-05       Impact factor: 3.590

7.  Lack of sexual dimorphism in femora of the eusocial and hypogonadic naked mole-rat: a novel animal model for the study of delayed puberty on the skeletal system.

Authors:  M Pinto; K J Jepsen; C J Terranova; R Buffenstein
Journal:  Bone       Date:  2009-09-15       Impact factor: 4.398

8.  Organizational role for pubertal androgens on adult hypothalamic-pituitary-adrenal sensitivity to testosterone in the male rat.

Authors:  O Evuarherhe; J D Leggett; E J Waite; Y M Kershaw; H C Atkinson; S L Lightman
Journal:  J Physiol       Date:  2009-04-29       Impact factor: 5.182

9.  Early interactions with mother and peers independently build adult social skills and shape BDNF and oxytocin receptor brain levels.

Authors:  Igor Branchi; James P Curley; Ivana D'Andrea; Francesca Cirulli; Frances A Champagne; Enrico Alleva
Journal:  Psychoneuroendocrinology       Date:  2012-08-19       Impact factor: 4.905

10.  Social structure predicts genital morphology in African mole-rats.

Authors:  Marianne L Seney; Diane A Kelly; Bruce D Goldman; Radim Sumbera; Nancy G Forger
Journal:  PLoS One       Date:  2009-10-15       Impact factor: 3.240

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