Adult Neural Plasticity in Naked Mole-Rats: Implications of Fossoriality, Longevity and Sociality on the Brain’s Capacity for Change

• Amrein I, Becker AS, Engler S, Huang SH, Müller J, Slomianka L, Oosthuizen MK (2014) Adult neurogenesis and its anatomical context in the hippocampus of three mole-rat species. Front Neuroanat 8:39

  Article  PubMed  PubMed Central  Google Scholar 

• Anacker A, Beery A (2013) Life in groups: the roles of oxytocin in mammalian sociality. Front Behav Neurosci 7:185

  Article  PubMed  PubMed Central  Google Scholar 

• Anderson GM, Relf HL, Rizwan MZ, Evans JJ (2008) Central and peripheral effects of RFamide-related peptide-3 on luteinizing hormone and prolactin secretion in rats. Endocrinol 150(4):1834–1840

  Article  CAS  Google Scholar 

• Azpurua J, Ke Z, Chen IX, Zhang Q, Ermolenko DN, Zhang ZD, Gorbunova V, Seluanov A (2013) Naked mole-rat has increased translational fidelity compared with the mouse, as well as a unique 28S ribosomal RNA cleavage. Proc Natl Acad Sci USA 110(43):17350–17355

  Google Scholar 

• Bakker J, Honda S, Harada N, Balthazart J (2003) The aromatase knockout (ArKO) mouse provides new evidence that estrogens are required for the development of the female brain. Ann N Y Acad Sci 1007(1):251–262

  Article  CAS  PubMed  Google Scholar 

• Barker JM, Wojtowicz JM, Boonstra R (2005) Where’s my dinner? Adult neurogenesis in free-living food-storing rodents. Genes Brain Behav 4(2):89–98

  Article  CAS  PubMed  Google Scholar 

• Beery AK, Zucker I (2010) Oxytocin and same-sex social behavior in female meadow voles. Neurosci 169(2):665–673

  Article  CAS  Google Scholar 

• Beery AK, Lacey EA, Francis DD (2008) Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J Comp Neurol 507(6):1847–1859

  Google Scholar 

• Beery AK, Bicks L, Mooney SJ, Goodwin NL, Holmes MM (2016) Sex, social status, and CRF receptor densities in naked mole-rats. J Comp Neurol 524(2):228–243

  Article  CAS  PubMed  Google Scholar 

• Ben-Jonathan N, Hnasko R (2001) Dopamine as a prolactin (PRL) inhibitor. Endocr Rev 22(6):724–763

  Article  CAS  PubMed  Google Scholar 

• Bickler PE, Fahlman CS, Taylor DM (2003) Oxygen sensitivity of NMDA receptors: relationship to NR2 subunit composition and hypoxia tolerance of neonatal neurons. Neurosci 118(1):25–35

  Article  CAS  Google Scholar 

• Bielsky IF, Young LJ (2004) Oxytocin, vasopressin, and social recognition in mammals. Peptides 25(9):1565–1574

  Article  CAS  PubMed  Google Scholar 

• Bingol B, Sheng M (2011) Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron 69(1):22–32

  Article  CAS  PubMed  Google Scholar 

• Bittman EL, Ehrlich DA, Ogdahl JL, Jetton AE (2003) Photoperiod and testosterone regulate androgen receptor immunostaining in the Siberian hamster brain. Biol Reprod 69(3):876–884

  Article  CAS  PubMed  Google Scholar 

• Blecher AS, Bennett NC, Medger K, Hagenah N, Ganswindt A, Oosthuizen MK (2020) Effect of colony disruption and social isolation on naked mole-rat endocrine correlates. Gen Comp Endocrinol 295:113520

  Google Scholar 

• Bonfanti L (2006) PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 80(3):129–164

  Article  CAS  PubMed  Google Scholar 

• Bonini NM (2002) Chaperoning brain degeneration. Proc Natl Acad Sci USA 99:16407–16411

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Breedlove SM, Arnold AP (1981) Sexually dimorphic motor nucleus in the rat lumbar spinal cord: response to adult hormone manipulation, absence in androgen-insensitive rats. Brain Res 225(2):297–307

  Article  CAS  PubMed  Google Scholar 

• Brett RA (1986) The Ecology and Behaviour of the Naked Mole-Rat, Heterocephalus glaber Ruppell (Rodenti: Bathyergidae). Dissertation, University College London, London, UK

  Google Scholar 

• Brett RA (1991) The ecology of naked mole-rat colonies: burrowing, food and limiting factors. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 137–184

  Google Scholar 

• Broeke JH, Roelandse M, Luteijn MJ, Boiko T, Matus A, Toonen RF, Verhage M (2010) Munc18 and Munc13 regulate early neurite outgrowth. Biol Cell 102(8):479–488

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Brom M, Both S, Laan E, Everaerd W, Spinhoven P (2014) The role of conditioning, learning and dopamine in sexual behavior: a narrative review of animal and human studies. Neurosci Biobehav Rev 38:38–59

  Article  CAS  PubMed  Google Scholar 

• Buffenstein R (2008) Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J Comp Physiol B 178(4):439–445

  Article  PubMed  Google Scholar 

• Buffenstein R, Craft W (2021) The idiosyncratic physiological traits of the naked mole-rat; a resilient animal model of aging, longevity, and healthspan. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 221–254

  Google Scholar 

• Campbell P, Ophir AG, Phelps SM (2009) Central vasopressin and oxytocin receptor distributions in two species of singing mice. J Comp Neurol 516(4):321–333

  Article  PubMed  Google Scholar 

• Catania KC, Remple MS (2002) Somatosensory cortex dominated by the representation of teeth in the naked mole-rat brain. Proc Natl Acad Sci 99(8):5692–5697

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Cavegn N, van Dijk RM, Menges D, Brettschneider H, Phalanndwa M, Chimimba CT et al (2013) Habitat-specific shaping of proliferation and neuronal differentiation in adult hippocampal neurogenesis of wild rodents. Front Neurosci 7(59)

  Google Scholar 

• Champagne FA, Curley JP (2016) Plasticity of the maternal brain across the lifespan. New Dir Child Adol Dev 2016(153):9–21

  Article  Google Scholar 

• Champagne FA, Weaver IC, Diorio J, Sharma S, Meaney MJ (2003) Natural variations in maternal care are associated with estrogen receptor α expression and estrogen sensitivity in the medial preoptic area. Endocrinol 144(11):4720–4724

  Article  CAS  Google Scholar 

• Choate JV, Resko JA (1992) Androgen receptor immunoreactivity in intact and castrate guinea pig using antipeptide antibodies. Brain Res 597(1):51–59

  Article  CAS  PubMed  Google Scholar 

• Choi DC, Furay AR, Evanson NK, Ulrich-Lai YM, Nguyen MM, Ostrander MM, Herman JP (2008) The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamic–pituitary–adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendocrinol 33(5):659–669

  Article  CAS  Google Scholar 

• Clancy AN, Whitman C, Michael RP, Albers HE (1994) Distribution of androgen receptor-like immunoreactivity in the brains of intact and castrated male hamsters. Brain Res Bull 33(3):325–332

  Article  CAS  PubMed  Google Scholar 

• Clarke FM, Faulkes CG (1997) Dominance and queen succession in captive colonies of the eusocial naked mole–rat, Heterocephalus glaber. Proc Roy Soc Lon B 264(1384):993–1000

  Google Scholar 

• Clarke FM, Faulkes CG (1998) Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole–rat, Heterocephalus glaber. Proc Roy Soc Lon B 265(1404):1391–1399

  Google Scholar 

• Clarke FM, Faulkes CG (2001) Intracolony aggression in the eusocial naked mole-rat, Heterocephalus glaber. Anim Behav 61(2):311–324

  Google Scholar 

• Clarke H, Dhillo WS, Jayasena CN (2015) Comprehensive review on kisspeptin and its role in reproductive disorders. Endocrinol Metab 30(2):124–141

  Article  CAS  Google Scholar 

• Coen CW, Bennett N, Holmes MM, Faulkes CG (2021) Neuropeptidergic and neuroendocrine systems underlying eusociality and the concomitant social regulation of reproduction in naked mole-rats: a comparative approach. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 59–103

  Google Scholar 

• Coolen LM, Peters HJ, Veening JG (1996) Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res 738(1):67–82

  Article  PubMed  Google Scholar 

• Costanzo MS, Bennett NC, Lutermann H (2009) Spatial learning and memory in African mole-rats: the role of sociality and sex. Physiol Behav 96(1):128–134

  Article  CAS  PubMed  Google Scholar 

• Davis-Walton J, Sherman PW (1994) Sleep arrhythmia in the eusocial naked mole-rat. Naturwissenschaften 81(6):272–275

  Article  CAS  PubMed  Google Scholar 

• De Vries GJ, Simerly RB (2002) Anatomy, development, and function of sexually dimorphic neural circuits in the mammalian brain. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Moss RL, Rubin RT (eds) Hormones, Brain and Behaviour: Development of Hormone-Dependent Neuronal Systems, vol IV. Academic, San Diego, pp 137–191

  Google Scholar 

• Dennis JC, Stilwell NK, Smith TD, Park TJ, Bhatnagar KP, Morrison EE (2020) Is the mole-rat vomeronasal organ functional? Anat Rec 303(2):318–329

  Google Scholar 

• Di Domenico F, Head E, Butterfield DA, Perluigi M (2014) Oxidative stress and proteostasis network: culprit and casualty of Alzheimer’s-like neurodegeneration. Adv Geriatrics 2014:527518

  Google Scholar 

• Döbrössy MD, Drapeau E, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2003) Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol Psych 8(12):974

  Article  Google Scholar 

• Donier E, Rugiero F, Jacob C, Wood JN (2008) Regulation of ASIC activity by ASIC4–new insights into ASIC channel function revealed by a yeast two-hybrid assay. Eur J Neurosci 28(1):74–86

  Article  PubMed  Google Scholar 

• Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2003) Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 100(24):4385–14390

  Article  CAS  Google Scholar 

• Du J, Reznikov LR, Price MP, Zha XM, Lu Y, Moninger TO, Wemmie JA, Welsh MJ (2014) Protons are a neurotransmitter that regulates synaptic plasticity in the lateral amygdala. Proc Natl Acad Sci USA 111(24):8961–8966

  Google Scholar 

• Ducret E, Anderson GM, Herbison AE (2009) RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone neuron firing in the mouse. Endocrinol 150(6):2799–2804

  Article  CAS  Google Scholar 

• Edrey YH, Casper D, Huchon D, Mele J, Gelfond JA, Kristan DM, Nevo E, Buffenstein R (2012) Sustained high levels of neuregulin-1 in the longest-lived rodents; a key determinant of rodent longevity. Aging Cell 11(2):213–222

  Google Scholar 

• Edrey YH, Medina DX, Gaczynska M, Osmulski PA, Oddo S, Caccamo A, Buffenstein R (2013) Amyloid beta and the longest-lived rodent: the naked mole-rat as a model for natural protection from Alzheimer’s disease. Neurobiol Aging 34(10):2352–2360

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Edwards PD, Mooney SJ, Bosson CO, Toor I, Palme R, Holmes MM, Boonstra R (2020) The stress of being alone: removal from the colony, but not social subordination, increases fecal cortisol metabolite levels in eusocial naked mole-rats. Horm Behav 121:104720

  Article  CAS  PubMed  Google Scholar 

• Endo M, Ohashi K, Sasaki Y, Goshima Y, Niwa R, Uemura T, Mizuno K (2003) Control of growth cone motility and morphology by LIM kinase and Slingshot via phosphorylation and dephosphorylation of cofilin. J Neurosci 23(7):2527–2537

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Evans RC, Morera-Herreras T, Cui Y, Du K, Sheehan T, Kotaleski JH et al (2012) The effects of NMDA subunit composition on calcium influx and spike timing-dependent plasticity in striatal medium spiny neurons. PLoS Comp Biol 8(4):e1002493

  Article  CAS  Google Scholar 

• Fang X, Seim I, Huang Z, Gerashchenko MV, Xiong Z et al (2014) Adaptations to a subterranean environment and longevity revealed by the analysis of mole-rat genomes. Cell Rep 8(5):1354–1364

  Google Scholar 

• Faulkes CG, Abbott DH (1991) Social control of reproduction in breeding and non-breeding male naked mole-rats (Heterocephalus glaber). Reproduction 93(2):427–435

  Google Scholar 

• Faulkes CG, Abbott DH (1993) Evidence that primer pheromones do not cause social suppression of reproduction in male and female naked mole-rats (Heterocephalus glaber). Reproduction 99(1):225–230

  Google Scholar 

• Faulkes CG, Abbott DH (1997) The physiology of a reproductive dictatorship: regulation of male and female reproduction by a single breeding female in colonies of naked mole-rats. In: Solomon NG, French JA (eds) Cooperative Breeding in Mammals. Cambridge University Press, Cambridge, pp 302–334

  Google Scholar 

• Faulkes CG, Bennett NC (2021) Social evolution in African mole-rats – a comparative overview. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 1–33

  Google Scholar 

• Faulkes CG, Abbott DH, Jarvis JUM (1990) Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber. Reproduction 88(2):559–568

  Google Scholar 

• Faykoo-Martinez M, Monks DA, Zovkic IB, Holmes MM (2018) Sex-and brain region-specific patterns of gene expression associated with socially-mediated puberty in a eusocial mammal. PLoS One 13(2):e0193417

  Article  PubMed  PubMed Central  CAS  Google Scholar 

• Featherstone DE, Davis WS, Dubreuil RR, Broadie K (2001) Drosophila α-and β-spectrin mutations disrupt presynaptic neurotransmitter release. J Neurosci 21(12):4215–4224

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Ferguson JN, Aldag JM, Insel TR, Young LJ (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21(20):8278–8285

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Forger NG (2009) The organizational hypothesis and final common pathways: sexual differentiation of the spinal cord and peripheral nervous system. Horm Behav 55(5):605–610

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Forger NG, Breedlove SM (1987) Seasonal variation in mammalian striated muscle mass and motoneuron morphology. J Neurobiol 18(2):155–165

  Article  CAS  PubMed  Google Scholar 

• Forger NG, Strahan JA, Castillo-Ruiz A (2016) Cellular and molecular mechanisms of sexual differentiation in the mammalian nervous system. Front Neuroendocrinol 40:67–86

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Fraley GS, Ulibarri CM (2002) Long-term castration effects motoneuron size but not number in the spinal nucleus of the bulbocavernosus in the adult male Mongolian gerbil. Brain Res 953(1–2):265–271

  Article  CAS  PubMed  Google Scholar 

• Francis DD, Champagne FC, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12(12):1145–1148

  Article  CAS  PubMed  Google Scholar 

• Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One 4(5):e5464

  Article  PubMed  PubMed Central  CAS  Google Scholar 

• Goodson JL, Schrock SE, Klatt JD, Kabelik D, Kingsbury MA (2009) Mesotocin and nonapeptide receptors promote estrildid flocking behavior. Science 325(5942):862–866

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39(5):749–765

  Article  CAS  PubMed  Google Scholar 

• Gründer S, Pusch M (2015) Biophysical properties of acid-sensing ion channels (ASICs). Neuropharmacology 94:9–18

  Article  PubMed  CAS  Google Scholar 

• Grune T, Catalgol B, Licht A, Ermak G, Pickering AM, Ngo JK, Davies KJ (2011) HSP70 mediates dissociation and reassociation of the 26S proteasome during adaptation to oxidative stress. Free Rad Biol Med 51(7):1355–1364

  Article  CAS  PubMed  Google Scholar 

• Hawkins LJ, Hadj-Moussa H, Nguyen VC, Pamenter ME, Storey KB (2019) Naked mole rats activate neuroprotective proteins during hypoxia. J Exp Zool A 331(10):571–576

  Article  CAS  Google Scholar 

• Healy K (2015) Eusociality but not fossoriality drives longevity in small mammals. Proc Roy Soc B 282(1806):20142917

  Article  Google Scholar 

• Healy K, Guillerme T, Finlay S, Kane A, Kelly SB, McClean D, Kelly DJ, Donohue I, Jackson AL, Cooper N (2014) Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc Roy Soc B 281(1784):20140298

  Google Scholar 

• Hebb DO (1949) The Organization of Behavior; A Neuropsychological Theory. Wiley, Oxford

  Google Scholar 

• Hegstrom CD, Jordan CL, Breedlove SM (2002) Photoperiod and androgens act independently to induce spinal nucleus of the bulbocavernosus neuromuscular plasticity in the Siberian hamster, Phodopus sungorus. J Neuroendocrinol 14(5):368–374

  Google Scholar 

• Hernandez D, Torres CA, Setlik W, Cebrián C, Mosharov EV et al (2012) Regulation of presynaptic neurotransmission by macroautophagy. Neuron 74(2):277–284

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Holmes MM, Goldman BD (2021) Social behavior in naked mole-rats: individual differences in phenotype and proximate mechanisms of mammalian eusociality. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 35–58

  Google Scholar 

• Holmes MM, Rosen GJ, Jordan CL, de Vries GJ, Goldman BD, Forger NG (2007) Social control of brain morphology in a eusocial mammal. Proc Natl Acad Sci 104(25):10548–10552

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Holmes MM, Goldman BD, Forger NG (2008) Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain. Horm Behav 54(2):278–285

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Holmes MM, Goldman BD, Goldman SL, Seney ML, Forger NG (2009) Neuroendocrinology and sexual differentiation in eusocial mammals. Front Neuroendocrinol 30(4):519–533

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Holmes MM, Seney ML, Goldman BD, Forger NG (2011) Social and hormonal triggers of neural plasticity in naked mole-rats. Behav Brain Res 218(1):234–239

  Article  CAS  PubMed  Google Scholar 

• Holmes MM, Van Mil S, Bulkowski C, Goldman SL, Goldman BD, Forger NG (2013) Androgen receptor distribution in the social decision-making network of eusocial naked mole-rats. Behav Brain Res 256:214–218

  Article  CAS  PubMed  Google Scholar 

• Holtze S, Braude S, Lemma A, Koch R, Morhart M, Szafranski K et al (2018) The microenvironment of naked mole-rat burrows in East Africa. Afr J Ecol 56(2):279–289

  Article  Google Scholar 

• Husson Z, Smith ESJ (2018) Naked mole-rat cortical neurons are resistant to acid-induced cell death. Mol Brain 11(1):26

  Article  PubMed  PubMed Central  CAS  Google Scholar 

• Insel TR, Shapiro LE (1992) Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc Natl Acad Sci USA 89(13):5981–5985

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Insel TR, Gelhard R, Shapiro LE (1991) The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice. Neurosci 43(2–3):623–630

  Article  CAS  Google Scholar 

• Jackman SL, Regehr WG (2017) The mechanisms and functions of synaptic facilitation. Neuron 94(3):447–464

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• James W (1890) The Principles of Psychology, vol 1. Henry Holt and Company, New York, p 109

  Google Scholar 

• Jarvis JUM (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212(4494):571–573

  Article  CAS  PubMed  Google Scholar 

• Jarvis JUM (1991) Reproduction of naked mole-rats. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, New Jersey, pp 384–425

  Google Scholar 

• Johansen K, Lykkeboe G, Weber RE, Maloiy GMO (1976) Blood respiratory properties in the naked mole-rat Heterocephalus glaber, a mammal of low body temperature. Resp Physiol 28(3):303–314

  Google Scholar 

• Johnson KM, Boonstra R, Wojtowicz JM (2010) Hippocampal neurogenesis in food-storing red squirrels: the impact of age and spatial behavior. Genes Brain Behav 9(6):583–591

  CAS  PubMed  Google Scholar 

• Kaiser S, Kruijver FP, Swaab DF, Sachser N (2003a) Early social stress in female guinea pigs induces a masculinization of adult behavior and corresponding changes in brain and neuroendocrine function. Behav Brain Res 144(1–2):199–210

  Article  CAS  PubMed  Google Scholar 

• Kaiser S, Kruijver FPM, Straub RH, Sachser N, Swaab DF (2003b) Early social stress in male guinea-pigs changes social behaviour, and autonomic and neuroendocrine functions. J Neuroendocrinol 15(8):761–769

  Article  CAS  PubMed  Google Scholar 

• Kalamatianos T, Faulkes CG, Oosthuizen MK, Poorun R, Bennett NC, Coen CW (2010) Telencephalic binding sites for oxytocin and social organization: a comparative study of eusocial naked mole-rats and solitary cape mole-rats. J Comp Neurol 518(10):1792–1813

  Article  CAS  PubMed  Google Scholar 

• Khan IU, Wallin R, Gupta RS, Kammer GM (1998) Protein kinase A-catalyzed phosphorylation of heat shock protein 60 chaperone regulates its attachment to histone 2B in the T lymphocyte plasma membrane. Proc Natl Acad Sci USA 95(18):10425–10430

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Klucken J, Shin Y, Masliah E, Hyman BT, McLean PJ (2004) Hsp70 reduces α-synuclein aggregation and toxicity. J Biol Chem 279(24):25497–25502

  Article  CAS  PubMed  Google Scholar 

• Konorski J (1948) Conditioned Reflexes and Neuron Organization. Cambridge University Press, Cambridge

  Google Scholar 

• Kourtis N, Tavernarakis N (2009) Autophagy and cell death in model organisms. Cell Death Diff 16(1):21

  Article  CAS  Google Scholar 

• Kramer PA, Duan J, Qian WJ, Marcinek DJ (2015) The measurement of reversible redox dependent post-translational modifications and their regulation of mitochondrial and skeletal muscle function. Front Physiol 6:347

  Article  PubMed  PubMed Central  Google Scholar 

• Lacey EA, Sherman PW (1991) Social organization of naked mole-rat colonies: evidence for division of labor. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 275–336

  Google Scholar 

• Laplante M, Sabatini DM (2009) mTOR signaling at a glance. J Cell Sci 122(20):3589–3594

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Larson J, Park TJ (2009) Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport 20(18):1634–1637

  Article  PubMed  Google Scholar 

• Laurie DJ, Bartke I, Schoepfer R, Naujoks K, Seeburg PH (1997) Regional, developmental and interspecies expression of the four NMDAR2 subunits, examined using monoclonal antibodies. Mol Brain Res 51(1–2):23–32

  Google Scholar 

• LaVinka PC, Brand A, Landau VJ, Wirtshafter D, Park TJ (2009) Extreme tolerance to ammonia fumes in African naked mole-rats: animals that naturally lack neuropeptides from trigeminal chemosensory nerve fibers. J Comp Physiol A 195(5):419

  Article  CAS  Google Scholar 

• Lee JM, Zipfel GJ, Choi DW (1999) The changing landscape of ischaemic brain injury mechanisms. Nature 399(6738):A7

  Article  CAS  PubMed  Google Scholar 

• Lee BP, Smith M, Buffenstein R, Harries LW (2020) Negligible senescence in naked mole-rats may be a consequence of well-maintained splicing regulation. GeroScience:1–19

  Google Scholar 

• Liang S, Mele J, Wu Y, Buffenstein R, Hornsby PJ (2010) Resistance to experimental tumorigenesis in cells of a long-lived mammal, the naked mole-rat (Heterocephalus glaber). Aging Cell 9(4):626–635

  Google Scholar 

• Lin SH, Chien YC, Chiang WW, Liu YZ, Lien CC, Chen CC (2015) Genetic mapping of ASIC 4 and contrasting phenotype to ASIC 1a in modulating innate fear and anxiety. Eur J Neurosci 41(12):1553–1568

  Article  PubMed  Google Scholar 

• Liu YC, Salamone JD, Sachs BD (1997) Impaired sexual response after lesions of the paraventricular nucleus of the hypothalamus in male rats. Behav Neurosci 111(6):1361

  Article  CAS  PubMed  Google Scholar 

• Maier T, Güell M, Serrano L (2009) Correlation of mRNA and protein in complex biological samples. FEBS Lett 583(24):3966–3973

  Article  CAS  PubMed  Google Scholar 

• Margulis SW, Saltzman W, Abbott DH (1995) Behavioral and hormonal changes in female naked mole-rats (Heterocephalus glaber) following removal of the breeding female from a colony. Horm Behav 29(2):227–247

  Google Scholar 

• Mazure NM, Pouysségur J (2010) Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol 22(2):177–180

  Article  CAS  PubMed  Google Scholar 

• McNab BK (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47(5):712–733

  Article  Google Scholar 

• Meberg PJ, Bamburg JR (2000) Increase in neurite outgrowth mediated by overexpression of actin depolymerizing factor. J Neurosci 20(7):2459–2469

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Mei L, Xiong WC (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 9(6):437

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Melen GJ, Pesce CG, Rossi MS, Kornblihtt AR (1999) Novel processing in a mammalian nuclear 28S pre-rRNA: tissue-specific elimination of an ‘intron’bearing a hidden break site. EMBO J 18(11):3107–3118

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Mizushima N (2007) Autophagy: process and function. Genes Dev 21(22):2861–2873

  Article  CAS  PubMed  Google Scholar 

• Mooney SJ, Holmes MM (2013) Social condition and oxytocin neuron number in the hypothalamus of naked mole-rats (Heterocephalus glaber). Neurosci 230:56–61

  Google Scholar 

• Mooney SJ, Douglas NR, Holmes MM (2014) Peripheral administration of oxytocin increases social affiliation in the naked mole-rat (Heterocephalus glaber). Horm Behav 65(4):380–385

  Google Scholar 

• Mooney SJ, Coen CW, Holmes MM, Beery AK (2015) Region-specific associations between sex, social status, and oxytocin receptor density in the brains of eusocial rodents. Neurosci 303:261–269

  Article  CAS  Google Scholar 

• Moudry P, Lukas C, Macurek L, Hanzlikova H, Hodny Z, Lukas J, Bartek J (2012) Ubiquitin-activating enzyme UBA1 is required for cellular response to DNA damage. Cell Cycle 11(8):1573–1582

  Article  CAS  PubMed  Google Scholar 

• Mulugeta E, Marion-Poll L, Gentien D, Ganswindt SB, Ganswindt A, Bennett NC et al (2017) Molecular insights into the pathways underlying naked mole-rat eusociality. bioRxiv:209932

  Google Scholar 

• Newman SW (1999) The medial extended amygdala in male reproductive behavior a node in the mammalian social behavior network. Ann N Y Acad Sci 877(1):242–257

  Article  CAS  PubMed  Google Scholar 

• Nicolopoulos-Stournaras S, Iles JF (1983) Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217(1):75–85

  Article  CAS  PubMed  Google Scholar 

• Nikoletopoulou V, Sidiropoulou K, Kallergi E, Dalezios Y, Tavernarakis N (2017) Modulation of autophagy by BDNF underlies synaptic plasticity. Cell Metab 26(1):230–242

  Article  CAS  PubMed  Google Scholar 

• Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS (1999) Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39(4):569–578

  Article  CAS  PubMed  Google Scholar 

• Northcutt KV, Lonstein JS (2008) Sex differences and effects of neonatal aromatase inhibition on masculine and feminine copulatory potentials in prairie voles. Horm Behav 54(1):160–169

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Nowak RM, Walker EP (1999) Walker’s Mammals of the World, vol 1. Johns Hopkins University Press, Baltimore

  Google Scholar 

• Nowak MA, Tarnita CE, Wilson EO (2010) The evolution of eusociality. Nature 466(7310):1057

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• O’Connell LA, Hofmann HA (2012) Evolution of a vertebrate social decision-making network. Science 336:1154–1157

  Article  PubMed  CAS  Google Scholar 

• Olazabal DE, Young LJ (2006a) Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Horm Behav 49(5):681–687

  Article  CAS  PubMed  Google Scholar 

• Olazabal DE, Young LJ (2006b) Oxytocin receptors in the nucleus accumbens facilitate “spontaneous” maternal behavior in adult female prairie voles. Neurosci 141(2):559–568

  Article  CAS  Google Scholar 

• Oomura Y, Aou S, Koyama Y, Fujita I, Yoshimatsu H (1988) Central control of sexual behavior. Brain Res Bull 20(6):863–870

  Article  CAS  PubMed  Google Scholar 

• Orr ME, Garbarino VR, Salinas A, Buffenstein R (2016) Extended postnatal brain development in the longest-lived rodent: prolonged maintenance of neotenous traits in the naked mole-rat brain. Front Neurosci 10:504

  Article  PubMed  PubMed Central  Google Scholar 

• Paillard J (1976) Réflexions sur l’usage du concept de plasticité en neurobiologie. J Psychologie 1:33–47

  Google Scholar 

• Pamenter ME, Lau GY, Richards JG, Milsom WK (2018) Naked mole rat brain mitochondria electron transport system flux and H+ leak are reduced during acute hypoxia. J Exp Biol 221(4):jeb171397

  PubMed  Google Scholar 

• Park KK, Luo X, Mooney SJ, Yungher BJ, Belin S, Wang C, Holmes MM, He Z (2017a) Retinal ganglion cell survival and axon regeneration after optic nerve injury in naked mole-rats. J Comp Neurol 525(2):380–388

  Google Scholar 

• Park TJ, Reznick J, Peterson BL, Blass G, Omerbašić D et al (2017b) Fructose-driven glycolysis supports anoxia resistance in the naked mole-rat. Science 356(6335):307–311

  Article  CAS  PubMed  Google Scholar 

• Park TJ, Smith ESJ, Reznick J, Bennett NC, Applegate DT, Larson J, Lewin GR (2021) African naked mole-rats demonstrate extreme tolerance to hypoxia and hypercapnia. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 255–269

  Google Scholar 

• Penz OK, Fuzik J, Kurek AB, Romanov R, Larson J, Park TJ, Harkany T, Keimpema E (2015) Protracted brain development in a rodent model of extreme longevity. Sci Rep 5:11592

  Google Scholar 

• Perachio AA, Marr LD, Alexander M (1979) Sexual behavior in male rhesus monkeys elicited by electrical stimulation of preoptic and hypothalamic areas. Brain Res 177(1):127–144

  Article  CAS  PubMed  Google Scholar 

• Peragine DE, Simpson JA, Mooney SJ, Lovern MB, Holmes MM (2014) Social regulation of adult neurogenesis in a eusocial mammal. Neurosci 268:10–20

  Article  CAS  Google Scholar 

• Peragine DE, Yousuf Y, Fu Y, Swift-Gallant A, Ginzberg K, Holmes MM (2016) Contrasting effects of opposite-versus same-sex housing on hormones, behavior and neurogenesis in a eusocial mammal. Horm Behav 81:28–37

  Article  CAS  PubMed  Google Scholar 

• Peragine DE, Pokarowski M, Mendoza-Viveros L, Swift-Gallant A, Cheng HYM, Bentley GE, Holmes MM (2017) RFamide-related peptide-3 (RFRP-3) suppresses sexual maturation in a eusocial mammal. Proc Natl Acad Sci 114(5):1207–1212

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Peroulakis ME, Goldman B, Forger NG (2002) Perineal muscles and motoneurons are sexually monomorphic in the naked mole-rat (Heterocephalus glaber). J Neurobiol 51(1):33–42

  Google Scholar 

• Peterson BL, Larson J, Buffenstein R, Park TJ, Fall CP (2012a) Blunted neuronal calcium response to hypoxia in naked mole-rat hippocampus. PLoS One 7(2):e31568

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Peterson BL, Park TJ, Larson J (2012b) Adult naked mole-rat brain retains the NMDA receptor subunit GluN2D associated with hypoxia tolerance in neonatal mammals. Neurosci Lett 506(2):342–345

  Article  CAS  PubMed  Google Scholar 

• Ramón y Cajal, S (1894) The Croonian lecture.—La fine structure des centres nerveux. Proc Roy Soc Lond 55(331–335):444–468

  Google Scholar 

• Rance NE, Krajewski SJ, Smith MA, Cholanian M, Dacks PA (2010) Neurokinin B and the hypothalamic regulation of reproduction. Brain Res 1364:116–128

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Riccio AP, Goldman BD (2000a) Circadian rhythms of locomotor activity in naked mole-rats (Heterocephalus glaber). Physiol Behav 71(1–2):1–13

  Google Scholar 

• Riccio AP, Goldman BD (2000b) Circadian rhythms of body temperature and metabolic rate in naked mole-rats. Physiol Behav 71(1–2):15–22

  Article  CAS  PubMed  Google Scholar 

• Rosen GJ, De Vries GJ, Goldman SL, Goldman BD, Forger NG (2007) Distribution of vasopressin in the brain of the eusocial naked mole-rat. J Comp Neurol 500(6):1093–1105

  Article  CAS  PubMed  Google Scholar 

• Rubinsztein DC, Mariño G, Kroemer G (2011) Autophagy and aging. Cell 146(5):682–695

  Article  CAS  PubMed  Google Scholar 

• Sar M, Lubahn DB, French FS, Wilson EM (1990) Immunohistochemical localization of the androgen receptor in rat and human tissues. Endocrinol 127(6):3180–3186

  Article  CAS  Google Scholar 

• Schneider JS, Stone MK, Wynne-Edwards KE, Horton TH, Lydon J, O’Malley B, Levine JE (2003) Progesterone receptors mediate male aggression toward infants. Proc Natl Acad Sci 100(5):2951–2956

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Schuhmacher LN, Smith ESJ (2016) Expression of acid-sensing ion channels and selection of reference genes in mouse and naked mole-rat. Mol Brain 9(1):97

  Google Scholar 

• Schwartz AL, Ciechanover A (1999) The ubiquitin-proteasome pathway and pathogenesis of human diseases. Ann Rev Med 50(1):57–74

  Article  CAS  PubMed  Google Scholar 

• Seney M, Goldman BD, Forger NG (2006) Breeding status affects motoneuron number and muscle size in naked mole-rats: recruitment of perineal motoneurons? J Neurobiol 66(12):1354–1364

  Article  PubMed  Google Scholar 

• Shah NM, Pisapia DJ, Maniatis S, Mendelsohn MM, Nemes A, Axel R (2004) Visualizing sexual dimorphism in the brain. Neuron 43(3):313–319

  Article  CAS  PubMed  Google Scholar 

• Sharma UR, Rissman EF (1994) Testosterone implants in specific neural sites activate female sexual behaviour. J Neuroendocrinol 6(4):423–432

  Article  CAS  PubMed  Google Scholar 

• Sherman PW, Jarvis JU, Braude SH (1992) Naked mole-rats. Sci Amer 267(2):72–78

  Article  Google Scholar 

• Simerly RB (2002) Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Ann Rev Neurosci 25(1):507–536

  Article  CAS  PubMed  Google Scholar 

• Simerly RB, Swanson LW, Chang C, Muramatsu M (1990) Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294(1):76–95

  Article  CAS  PubMed  Google Scholar 

• Singh P, Krishna A, Sridaran R, Tsutsui K (2011) Immunohistochemical localization of GnRH and RFamide-related peptide-3 in the ovaries of mice during the estrous cycle. J Mol Histol 42(5):371

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neurosci 130(4):843–852

  Article  CAS  Google Scholar 

• Song G, Ouyang G, Bao S (2005) The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med 9(1):59–71

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Stram AR, Payne RM (2016) Post-translational modifications in mitochondria: protein signaling in the powerhouse. Cell Mol Life Sci 73(21):4063–4073

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21(8):323–331

  Article  CAS  PubMed  Google Scholar 

• Swift-Gallant A, Mo K, Peragine DE, Monks DA, Holmes MM (2015) Removal of reproductive suppression reveals latent sex differences in brain steroid hormone receptors in naked mole-rats, Heterocephalus glaber. Biol Sex Diff 6(1):31

  Google Scholar 

• Taylor JS, Bampton ET (2004) Factors secreted by Schwann cells stimulate the regeneration of neonatal retinal ganglion cells. J Anat 204(1):25–31

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Toor I, Clement D, Carlson EN, Holmes MM (2015) Olfaction and social cognition in eusocial naked mole-rats, Heterocephalus glaber. Anim Behav 107:175–181

  Google Scholar 

• Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK et al (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62(3):405–496

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Triplett JC, Tramutola A, Swomley A, Kirk J, Grimes K et al (2015) Age-related changes in the proteostasis network in the brain of the naked mole-rat: implications promoting healthy longevity. Biochimica et Biophysica Acta (BBA)-Mol Basis Dis 1852(10):2213–2224

  Article  CAS  Google Scholar 

• Triplett JC, Swomley AM, Kirk J, Grimes KM, Lewis KN et al (2016) Reaching out to send a message: proteins associated with neurite outgrowth and neurotransmission are altered with age in the long-lived naked mole-rat. Neurochem Res 41(7):1625–1634

  Article  CAS  PubMed  Google Scholar 

• Unger EK, Burke KJ Jr, Yang CF, Bender KJ, Fuller PM, Shah NM (2015) Medial amygdalar aromatase neurons regulate aggression in both sexes. Cell Rep 10(4):453–462

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR (1998) Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79(2):555–566

  Google Scholar 

• Wasling P, Hanse E, Gustafsson B (2004) Developmental changes in release properties of the CA3-CA1 glutamate synapse in rat hippocampus. J Neurophysiol 92(5):2714–2724

  Article  CAS  PubMed  Google Scholar 

• Wemmie JA, Chen J, Askwith CC, Hruska-Hageman AM, Price MP et al (2002) The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34(3):463–477

  Article  CAS  PubMed  Google Scholar 

• Will B, Dalrymple-Alford J, Wolff M, Cassel JC (2008) The concept of brain plasticity—Paillard’s systemic analysis and emphasis on structure and function (followed by the translation of a seminal paper by Paillard on plasticity). Behav Brain Res 192(1):2–7

  Article  PubMed  Google Scholar 

• Williams SA, Shattuck MR (2015) Ecology, longevity and naked mole-rats: confounding effects of sociality? Proc Roy Soc B 282(1802):20141664

  Google Scholar 

• Witt DM, Insel TR (1994) Increased Fos expression in oxytocin neurons following masculine sexual behavior. J Neuroendocrinol 6(1):13–18

  Article  CAS  PubMed  Google Scholar 

• Wong E, Cuervo AM (2010) Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 13(7):805

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Wynne-Edwards KE, Timonin ME (2007) Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Horm Behav 52(1):114–121

  Article  CAS  PubMed  Google Scholar 

• Xiao B, Wang S, Yang G, Sun X, Zhao S et al (2017) HIF-1α contributes to hypoxia adaptation of the naked mole-rat. Oncotarget 8(66):109941

  Google Scholar 

• Xie Y, Vessey JP, Konecna A, Dahm R, Macchi P, Kiebler MA (2007) The GTP-binding protein Septin 7 is critical for dendrite branching and dendritic-spine morphology. Curr Biol 17(20):1746–1751

  Article  CAS  PubMed  Google Scholar 

• Xu J, He L, Wu LG (2007) Role of Ca2+ channels in short-term synaptic plasticity. Curr Op Neurobiol 17(3):352–359

  Article  CAS  PubMed  Google Scholar 

• Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ, Semenza GL (2008) Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 283(16):10892–10903

  Google Scholar 

• Zhao S, Lin L, Kan G, Xu C, Tang Q et al (2014) High autophagy in the naked mole-rat may play a significant role in maintaining good health. Cell Physiol Biochem 33(2):321–332

  Google Scholar 

• Zhou S, Holmes MM, Forger NG, Goldman BD, Lovern MB, Caraty A, Kalló I, Faulkes CG, Coen CW (2013) Socially regulated reproductive development: analysis of GnRH-1 and kisspeptin neuronal systems in cooperatively breeding naked mole-rats (Heterocephalus glaber). J Comp Neurol 521(13):3003–3029

  Google Scholar 

Download references