Russ Edward Carpenter

All Publications

• Nuance and behavioral cogency: How the Visible Burrow System inspired the Stress-Alternatives Model and conceptualization of the continuum of anxiety PHYSIOLOGY & BEHAVIOR Robertson, J. M., Prince, M. A., Achua, J. K., Carpenter, R. E., Arendt, D. H., Smith, J. P., Summers, T. L., Summers, T. R., Summers, C. H. 2015; 146: 86-97

  View details for DOI 10.1016/j.physbeh.2015.03.036

  View details for Web of Science ID 000356208300012

• Social status differences regulate the serotonergic system of a cichlid fish, Astatotilapia burtoni. journal of experimental biology Loveland, J. L., Uy, N., Maruska, K. P., Carpenter, R. E., Fernald, R. D. 2014; 217: 2680-2690

  Abstract

  Serotonin (5-HT) inhibits aggression and modulates aspects of sexual behaviour in many species, but the mechanisms responsible are not well understood. Here, we exploited the social dominance hierarchy of Astatotilapia burtoni to understand the role of the serotonergic system in long-term maintenance of social status. We identified three populations of 5-HT cells in dorsal and ventral periventricular pretectal nuclei (PPd, PPv), the nucleus of the paraventricular organ (PVO) and raphe. Dominant males had more 5-HT cells than subordinates in the raphe, but the size of these cells did not differ between social groups. Subordinates had higher serotonergic turnover in the raphe and preoptic area (POA), a nucleus essential for hypothalamic-pituitary-gonadal (HPG) axis function. The relative abundance of mRNAs for 5-HT receptor (5-HTR) subtypes 1A and 2A (htr1a, htr2a) was higher in subordinates, a difference restricted to the telencephalon. Because social status is tightly linked to reproductive capacity, we asked whether serotonin turnover and the expression of its receptors correlated with testes size and circulating levels of 11-ketotestosterone (11-KT). We found negative correlations between both raphe and POA serotonin turnover and testes size, as well as between htr1a mRNA levels and circulating 11-KT. Thus, increased serotonin turnover in non-aggressive males is restricted to specific brain nuclei and is associated with increased expression of 5-HTR subtypes 1A and 2A exclusively in the telencephalon.

  View details for DOI 10.1242/jeb.100685

  View details for PubMedID 24855673

• Social Opportunity Rapidly Regulates Expression of CRF and CRF Receptors in the Brain during Social Ascent of a Teleost Fish, Astatotilapia burtoni. PloS one Carpenter, R. E., Maruska, K. P., Becker, L., Fernald, R. D. 2014; 9 (5): e96632

  Abstract

  In social animals, hierarchical rank governs food availability, territorial rights and breeding access. Rank order can change rapidly and typically depends on dynamic aggressive interactions. Since the neuromodulator corticotrophin releasing factor (CRF) integrates internal and external cues to regulate the hypothalamic-pituitary adrenal (HPA) axis, we analyzed the CRF system during social encounters related to status. We used a particularly suitable animal model, African cichlid fish, Astatotilapia burtoni, whose social status regulates reproduction. When presented with an opportunity to rise in rank, subordinate A. burtoni males rapidly change coloration, behavior, and their physiology to support a new role as dominant, reproductively active fish. Although changes in gonadotropin-releasing hormone (GnRH1), the key reproductive molecular actor, have been analyzed during social ascent, little is known about the roles of CRF and the HPA axis during transitions. Experimentally enabling males to ascend in social rank, we measured changes in plasma cortisol and the CRF system in specific brain regions 15 minutes after onset of social ascent. Plasma cortisol levels in ascending fish were lower than subordinate conspecifics, but similar to levels in dominant animals. In the preoptic area (POA), where GnRH1 cells are located, and in the pituitary gland, CRF and CRF1 receptor mRNA levels are rapidly down regulated in ascending males compared to subordinates. In the Vc/Vl, a forebrain region where CRF cell bodies are located, mRNA coding for both CRFR1 and CRFR2 receptors is lower in ascending fish compared to stable subordinate conspecifics. The rapid time course of these changes (within minutes) suggests that the CRF system is involved in the physiological changes associated with shifts in social status. Since CRF typically has inhibitory effects on the neuroendocrine reproductive axis in vertebrates, this attenuation of CRF activity may allow rapid activation of the reproductive axis and facilitate the transition to dominance.

  View details for DOI 10.1371/journal.pone.0096632

  View details for PubMedID 24824619

  View details for PubMedCentralID PMC4019471

• Characterization of cell proliferation throughout the brain of the African cichlid fish Astatotilapia burtoni and its regulation by social status JOURNAL OF COMPARATIVE NEUROLOGY Maruska, K. P., Carpenter, R. E., Fernald, R. D. 2012; 520 (15): 3471-3491

  Abstract

  New cells are added in the brains of all adult vertebrates, but fishes have some of the greatest potential for neurogenesis and gliogenesis among all taxa, partly due to their indeterminate growth. Little is known, however, about how social interactions influence cell proliferation in the brain of these fishes that comprise the largest group of vertebrates. We used 5-bromo-2'-deoxyuridine (BrdU) to identify and localize proliferation zones in the telencephalon, diencephalon, mesencephalon, and rhombencephalon that were primarily associated with ventricular surfaces in the brain of the African cichlid fish Astatotilapia burtoni. Cell migration was evident in some regions by 1 day post injection, and many newborn cells coexpressed the neuronal marker HuC/D at 30 days, suggesting they had differentiated into neurons. To test the hypothesis that social status and perception of an opportunity to rise in rank influenced cell proliferation, we compared numbers of BrdU-labeled cells in multiple brain nuclei among fish of different social status. Socially suppressed subordinate males had the lowest numbers of proliferating cells in all brain regions examined, but males that were given an opportunity to rise in status had higher cell proliferation rates within 1 day, suggesting rapid upregulation of brain mitotic activity associated with this social transition. Furthermore, socially isolated dominant males had similar numbers of BrdU-labeled cells compared with dominant males that were housed in a socially rich environment, suggesting that isolation has little effect on proliferation and that reduced proliferation in subordinates is a result of the social subordination. These results suggest that A. burtoni will be a useful model to analyze the mechanisms of socially induced neurogenesis in vertebrates.

  View details for DOI 10.1002/cne.23100

  View details for Web of Science ID 000307849400009

  View details for PubMedID 22431175

• Food deprivation explains effects of mouthbrooding on ovaries and steroid hormones, but not brain neuropeptide and receptor mRNAs, in an African cichlid fish HORMONES AND BEHAVIOR Grone, B. P., Carpenter, R. E., Lee, M., Maruska, K. P., Fernald, R. D. 2012; 62 (1): 18-26

  Abstract

  Feeding behavior and reproduction are coordinately regulated by the brain via neurotransmitters, circulating hormones, and neuropeptides. Reduced feeding allows animals to engage in other behaviors important for fitness, including mating and parental care. Some fishes cease feeding for weeks at a time in order to provide care to their young by brooding them inside the male or female parent's mouth. Maternal mouthbrooding is known to impact circulating hormones and subsequent reproductive cycles, but neither the full effects of food deprivation nor the neural mechanisms are known. Here we ask what effects mouthbrooding has on several physiological processes including gonad and body mass, brain neuropeptide and receptor gene expression, and circulating steroid hormones in a mouthbrooding cichlid species, Astatotilapia burtoni. We ask whether any observed changes can be explained by food deprivation, and show that during mouthbrooding, ovary size and circulating levels of androgens and estrogens match those seen during food deprivation. Levels of gonadotropin-releasing hormone 1 (GnRH1) mRNA in the brain were low in food-deprived females compared to controls and in mouthbrooding females compared to gravid females. Levels of mRNA encoding two peptides involved in regulating feeding, hypocretin and cholecystokinin, were increased in the brains of food-deprived females. Brain mRNA levels of two receptors, GnRH receptor 2 and NPY receptor Y8c, were elevated in mouthbrooding females compared to the fed condition, but NPY receptor Y8b mRNA was differently regulated by mouthbrooding. These results suggest that many, but not all, of the characteristic physiological changes that occur during mouthbrooding are consequences of food deprivation.

  View details for DOI 10.1016/j.yhbeh.2012.04.012

  View details for Web of Science ID 000305818500003

  View details for PubMedID 22561338

  View details for PubMedCentralID PMC3379815

• Glucocorticoid interaction with aggression in non-mammalian vertebrates: Reciprocal action 4th Spring Meeting of the European Journal of Pharmacology Summers, C. H., Watt, M. J., Ling, T. L., Forster, G. L., Carpenter, R. E., Korzan, W. J., Lukkes, J. L., Overli, O. ELSEVIER SCIENCE BV. 2005: 21–35

  Abstract

  Socially aggressive interaction is stressful, and as such, glucocorticoids are typically secreted during aggressive interaction in a variety of vertebrates, which may both potentiate and inhibit aggression. The behavioral relationship between corticosterone and/or cortisol in non-mammalian (as well as mammalian) vertebrates is dependent on timing, magnitude, context, and coordination of physiological and behavioral responses. Chronically elevated plasma glucocorticoids reliably inhibit aggressive behavior, consistent with an evolutionarily adaptive behavioral strategy among subordinate and submissive individuals. Acute elevation of plasma glucocorticoids may either promote an actively aggressive response via action in specialized local regions of the brain such as the anterior hypothalamus, or is permissive to escalated aggression and/or activity. Although the permissive effect of glucocorticoids on aggression does not suggest an active role for the hormone, the corticosteroids may be necessary for full expression of aggressive behavior, as in the lizard Anolis carolinensis. These effects suggest that short-term stress may generally be best counteracted by an actively aggressive response, at least for socially dominant proactive individuals. An acute and active response may be evolutionarily maladaptive under chronic, uncontrollable and unpredictable circumstances. It appears that subordinate reactive individuals often produce compulsorily chronic responses that inhibit aggression and promote submissive behavior.

  View details for DOI 10.1016/j.ejphar.2005.09.059

  View details for Web of Science ID 000233958700004

  View details for PubMedID 16298361