Social and hormonal triggers of neural plasticity in naked mole-rats

Abstract

Naked mole-rats are eusocial rodents that live in large social groups with a strict reproductive hierarchy. In each colony only a few individuals breed; all others are non-reproductive subordinates. We previously showed that breeders have increased volume of several brain regions linked to reproduction: the paraventricular nucleus of the hypothalamus (PVN), the principal nucleus of the bed nucleus of the stria terminalis (BSTp), and the medial amygdala (MeA). Breeders also have more large motoneurons in Onuf's nucleus (ON) in the spinal cord, a cell group innervating perineal muscles that attach to the genitalia. Here, we sought to determine triggers for the neural changes seen in breeders. Specifically, we compared four groups of animals: subordinates, paired animals that did not reproduce, gonadally intact breeders, and gonadectomized breeders. We find that pairing alone is sufficient to cause breeder-like changes in volume of the PVN and cell size distribution in ON. In contrast, increases in BSTp volume were seen only in animals that actually reproduced. Those changes that were seen in successful breeders appear to be independent of gonadal steroids because long-term gonadectomy did not reverse the breeder-like neural changes in the PVN, BSTp or ON, although a trend for gonadectomized animals having larger MeA volumes was detected. Thus, neural changes associated with breeding status in naked mole-rats may be triggered by different aspects of the social and reproductive environment; once changes occur they are largely independent of gonadal hormones and may be permanent.

Social regulation of adult neurogenesis in a eusocial mammal

“…Furthermore, DCX expression was comparable among intact and GDX opposite-sex pair housed subordinates. The apparent independence of adult neurogenesis from gonadal factors in this species is intriguing, and corresponds with prior reports that status related changes in naked mole-rat brain morphology are not reversed by long-term gonadectomy (Holmes et al, 2011). Findings also line up with research demonstrating that the impact of gonadal status on hippocampal neurogenesis is dictated by the duration of time a rodent has been deprived of normal circulating levels of gonadal hormones.…”

“…Likewise, colonyhoused subordinates may become breeders if sexual suppression is lifted by a former breeder's death or removal (Margulis et al, 1995;Clarke and Faulkes, 1997). Though pronounced alterations in neural and endocrine functions accompany the change (Faulkes et al, 1990a;Margulis et al, 1995;Clarke and Faulkes, 1997;Seney et al, 2006;Holmes et al, 2008;Holmes et al, 2011;Mooney and Holmes, 2013), many or all subordinates are capable of transitioning to breeding status under the appropriate social conditions. This striking behavioural and physiological plasticity displayed by otherwise mature subordinates makes the naked mole-rat a prime candidate for the study of adult neurogenesis.…”

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

“…In colonies of up to 300 individuals, breeding is restricted to one dominant female (the queen) and one to three males, with other colony members being socially subordinate and reproductively suppressed. Though pronounced alterations in neural and endocrine function accompany the change (37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47), male and female subordinates are capable of transitioning to breeding status following the death/removal of breeders or separation from the colony. Indeed, although colony-housed subordinates have low progesterone (P), testosterone (T), and luteinizing hormone (LH) concentrations compared with same-sex breeders (37,38), they show elevated urinary P and T levels within 1 wk of separation from the colony (37,40), with females developing a perforated vagina during that time (37).…”

Hormones, reproduction and disease in the longest-lived rodent: the naked mole rat

“…18 Eusociality may be correlated with a relative lack of sex differences and a reduced influence of gonadal hormones (androgens, estrogens) on some functions to which these hormones are usually tightly linked. 19,20 Changes in behavior, in brain anatomy and even in female body morphology accompany changes in social and reproductive status in NMR, [20][21][22] and this may be dependent or not of gonadal hormonal changes. 19,[22][23][24] Members of a NMR colony work cooperatively and sleep together in large huddles.…”

“…19,20 Changes in behavior, in brain anatomy and even in female body morphology accompany changes in social and reproductive status in NMR, [20][21][22] and this may be dependent or not of gonadal hormonal changes. 19,[22][23][24] Members of a NMR colony work cooperatively and sleep together in large huddles. They exhibit very low levels of aggression to other colony members, yet are fiercely xenophobic and will mount vigorous attacks against intruders in the laboratory setting.…”