Socially regulated reproductive development: Analysis of GnRH‐1 and kisspeptin neuronal systems in cooperatively breeding naked mole‐rats (Heterocephalus glaber)

In naked mole‐rat (NMR) colonies, breeding is monopolized by the queen and her consorts. Subordinates experience gonadal development if separated from the queen. To elucidate the neuroendocrine factors underlying reproductive suppression/development in NMRs, we quantified plasma gonadal steroids and GnRH‐1‐ and kisspeptin‐immunoreactive (ir) neurons in subordinate adults and in those allowed to develop into breeders, with or without subsequent gonadectomy. In males and females, respectively, plasma testosterone and progesterone are higher in breeders than in subordinates. No such distinction occurs for plasma estradiol; its presence after gonadectomy and its positive correlation with adrenal estradiol suggest an adrenal source. Numbers of GnRH‐1‐ir cell bodies do not differ between gonad‐intact breeders and subordinates within or between the sexes. As in phylogenetically related guinea pigs, kisspeptin‐ir processes pervade the internal and external zones of the median eminence. Their distribution is consistent with actions on GnRH‐1 neurons at perikaryal and/or terminal levels. In previously investigated species, numbers of kisspeptin‐ir cell bodies vary from substantial to negligible according to sex and/or reproductive state. NMRs are exceptional: irrespective of sex, reproductive state, or presence of gonads, substantial numbers of kisspeptin‐ir cell bodies are detected in the rostral periventricular region of the third ventricle (RP3V) and in the anterior periventricular (PVa), arcuate, and dorsomedial hypothalamic nuclei. Nevertheless, the greater number in the RP3V/PVa of female breeders compared with female subordinates or male breeders suggests that emergence from a hypogonadotrophic state in females may involve kisspeptin‐related mechanisms similar to those underlying puberty or seasonal breeding in other species. J. Comp. Neurol. 521: 3003–3029, 2013. © 2013 Wiley Periodicals, Inc.

[1]  A. Kauffman,et al.  Organizational and activational effects of sex steroids on kisspeptin neuron development , 2013, Frontiers in Neuroendocrinology.

[2]  R. Goodman,et al.  Kisspeptin neurons from mice to men: similarities and differences. , 2012, Endocrinology.

[3]  O. Rønnekleiv,et al.  Kisspeptin expression in guinea pig hypothalamus: Effects of 17β‐estradiol , 2012, The Journal of comparative neurology.

[4]  M. Tena-Sempere,et al.  Kisspeptins and reproduction: physiological roles and regulatory mechanisms. , 2012, Physiological reviews.

[5]  Z. Liposits,et al.  Co‐Localisation of Kisspeptin with Galanin or Neurokinin B in Afferents to Mouse GnRH Neurones , 2012, Journal of neuroendocrinology.

[6]  George M. Church,et al.  RNA Sequencing Reveals Differential Expression of Mitochondrial and Oxidation Reduction Genes in the Long-Lived Naked Mole-Rat When Compared to Mice , 2011, PloS one.

[7]  H. Patisaul,et al.  Sexually dimorphic expression of hypothalamic estrogen receptors α and β and kiss1 in neonatal male and female rats , 2011, The Journal of comparative neurology.

[8]  L. Peshkin,et al.  Genome sequencing reveals insights into physiology and longevity of the naked mole rat , 2011, Nature.

[9]  N. Inoue,et al.  Kisspeptin neurons mediate reflex ovulation in the musk shrew (Suncus murinus) , 2011, Proceedings of the National Academy of Sciences.

[10]  A. Herbison,et al.  Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. , 2011, Endocrinology.

[11]  B. Goldman,et al.  Social and hormonal triggers of neural plasticity in naked mole-rats , 2011, Behavioural Brain Research.

[12]  Joshua Kim,et al.  Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. , 2011, Endocrinology.

[13]  M. Keller,et al.  Mapping of Kisspeptin Fibres in the Brain of the Pro‐Oestrous Rat , 2010, Journal of neuroendocrinology.

[14]  Z. Liposits,et al.  Evidence for Suprachiasmatic Vasopressin Neurones Innervating Kisspeptin Neurones in the Rostral Periventricular Area of the Mouse Brain: Regulation by Oestrogen , 2010, Journal of neuroendocrinology.

[15]  F. Ebling Photoperiodic regulation of puberty in seasonal species , 2010, Molecular and Cellular Endocrinology.

[16]  S. Han,et al.  Neurobiological mechanisms underlying kisspeptin activation of gonadotropin-releasing hormone (GnRH) neurons at puberty , 2010, Molecular and Cellular Endocrinology.

[17]  A. Kauffman,et al.  Sexual differentiation and development of forebrain reproductive circuits , 2010, Current Opinion in Neurobiology.

[18]  W. Colledge,et al.  The role of kisspeptin signaling in reproduction. , 2010, Physiology.

[19]  C. G. Faulkes,et al.  Telencephalic binding sites for oxytocin and social organization: A comparative study of eusocial naked mole‐rats and solitary cape mole‐rats , 2010, The Journal of comparative neurology.

[20]  A. Juul,et al.  Maturation of kisspeptinergic neurons coincides with puberty onset in male rats , 2010, Peptides.

[21]  H. Matsumoto,et al.  Significance of Neonatal Testicular Sex Steroids to Defeminize Anteroventral Periventricular Kisspeptin Neurons and the GnRH/LH Surge System in Male Rats1 , 2009, Biology of reproduction.

[22]  Joshua Kim,et al.  Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty. , 2009, American journal of physiology. Endocrinology and metabolism.

[23]  B. Goldman,et al.  Social Structure Predicts Genital Morphology in African Mole-Rats , 2009, PloS one.

[24]  K. Mogi,et al.  Gonadotrophin‐Releasing Hormone Pulse Generator Activity in the Hypothalamus of the Goat , 2009, Journal of neuroendocrinology.

[25]  R. Steiner,et al.  Kisspeptin signaling in the brain. , 2009, Endocrine reviews.

[26]  M. Holmes,et al.  Neuroendocrinology and sexual differentiation in eusocial mammals , 2009, Frontiers in Neuroendocrinology.

[27]  W. Colledge,et al.  Distribution of Kisspeptin Neurones in the Adult Female Mouse Brain , 2009, Journal of neuroendocrinology.

[28]  C. Foradori,et al.  Biological and anatomical evidence for kisspeptin regulation of the hypothalamic-pituitary-gonadal axis of estrous horse mares. , 2009, Endocrinology.

[29]  H. Matsumoto,et al.  Possible Role of Oestrogen in Pubertal Increase of Kiss1/Kisspeptin Expression in Discrete Hypothalamic Areas of Female Rats , 2009, Journal of neuroendocrinology.

[30]  I. Franceschini,et al.  Kisspeptin immunoreactive neurons in the equine hypothalamus Interactions with GnRH neuronal system , 2008, Journal of Chemical Neuroanatomy.

[31]  L. Kriegsfeld,et al.  Photoperiod and Testosterone Interact to Drive Seasonal Changes in Kisspeptin Expression in Siberian Hamsters (Phodopus sungorus) , 2008, Journal of neuroendocrinology.

[32]  M. Oosthuizen,et al.  An immunohistochemical study of the gonadotrophin-releasing hormone 1 system in solitary Cape mole-rats, Georychus capensis, and social Natal mole-rats, Cryptomys hottentotus natalensis , 2008, Neuroscience.

[33]  M. O'Riain,et al.  Neuroanatomical investigation of the gonadotrophin-releasing hormone 1 system in the seasonally breeding Cape dune mole-rat, Bathyergus suillus , 2008, Brain Research Bulletin.

[34]  J. D. Hahn,et al.  Fasting Reduces KiSS‐1 Expression in the Anteroventral Periventricular Nucleus (AVPV): Effects of Fasting on the Expression of KiSS‐1 and Neuropeptide Y in the AVPV or Arcuate Nucleus of Female Rats , 2008, Journal of neuroendocrinology.

[35]  W. Colledge,et al.  Kisspeptin–GPR54 Signaling Is Essential for Preovulatory Gonadotropin-Releasing Hormone Neuron Activation and the Luteinizing Hormone Surge , 2008, The Journal of Neuroscience.

[36]  B. Goldman,et al.  Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain , 2008, Hormones and Behavior.

[37]  K. Guerriero,et al.  Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy. , 2008, Endocrinology.

[38]  A. Herbison,et al.  Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: The case for the rostral periventricular area of the third ventricle (RP3V) , 2008, Brain Research Reviews.

[39]  R. Buffenstein Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species , 2008, Journal of Comparative Physiology B.

[40]  L. Kriegsfeld,et al.  Suppression of kisspeptin expression and gonadotropic axis sensitivity following exposure to inhibitory day lengths in female Siberian hamsters , 2007, Hormones and Behavior.

[41]  Felecia Cerrato,et al.  Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice. , 2007, Endocrinology.

[42]  Cynthia L. Jordan,et al.  Social control of brain morphology in a eusocial mammal , 2007, Proceedings of the National Academy of Sciences.

[43]  W. Colledge,et al.  Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene , 2007, Proceedings of the National Academy of Sciences.

[44]  R. Steiner,et al.  Sexual differentiation of Kiss1 gene expression in the brain of the rat. , 2007, Endocrinology.

[45]  H. Matsumoto,et al.  Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. , 2007, The Journal of reproduction and development.

[46]  P. Pévet,et al.  Kisspeptin: A key link to seasonal breeding , 2007, Reviews in Endocrine and Metabolic Disorders.

[47]  C. Clay,et al.  KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. , 2007, Endocrinology.

[48]  L. Kriegsfeld,et al.  Environmental control of kisspeptin: implications for seasonal reproduction. , 2007, Endocrinology.

[49]  B. Goldman,et al.  Breeding status affects motoneuron number and muscle size in naked mole-rats: recruitment of perineal motoneurons? , 2006, Journal of neurobiology.

[50]  A. Herbison,et al.  Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. , 2006, Endocrinology.

[51]  G. Delsol,et al.  Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha , 2006, Neuroscience Letters.

[52]  R. Steiner,et al.  Kiss1 Neurons in the Forebrain as Central Processors for Generating the Preovulatory Luteinizing Hormone Surge , 2006, The Journal of Neuroscience.

[53]  B. Goldman,et al.  Influence of gonadal sex hormones on behavioral components of the reproductive hierarchy in naked mole-rats , 2006, Hormones and Behavior.

[54]  R. Steiner,et al.  Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. , 2006, Reproduction.

[55]  A. Katz,et al.  Relations between social status and the gonadotrophin‐releasing hormone system in females of two cooperatively breeding species of African mole‐rats, Cryptomys hottentotus hottentotus and Cryptomys hottentotus pretoriae: Neuroanatomical and neuroendocrinological studies , 2006, The Journal of comparative neurology.

[56]  H. Matsumoto,et al.  Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. , 2005, Endocrinology.

[57]  R. Steiner,et al.  Regulation of Kiss1 gene expression in the brain of the female mouse. , 2005, Endocrinology.

[58]  R. Braun,et al.  Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. , 2005, Endocrinology.

[59]  E. Hrabovszky,et al.  Characterization of Gonadotrophin‐Releasing Hormone Precursor cDNA in the Old World Mole‐Rat Cryptomys Hottentotus Pretoriae: High Degree of Identity with the New World Guinea Pig Sequence , 2005, Journal of neuroendocrinology.

[60]  F. Casanueva,et al.  Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. , 2005, Endocrinology.

[61]  S. Ojeda,et al.  Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[62]  D. Ma,et al.  Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[63]  R. Steiner,et al.  Kisspeptin Activation of Gonadotropin Releasing Hormone Neurons and Regulation of KiSS-1 mRNA in the Male Rat , 2005, Neuroendocrinology.

[64]  H. Matsumoto,et al.  Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. , 2004, Biochemical and biophysical research communications.

[65]  Imre Kalló,et al.  Expression of VIP and/or PACAP receptor mRNA in peptide synthesizing cells within the suprachiasmatic nucleus of the rat and in its efferent target sites , 2004, The Journal of comparative neurology.

[66]  S. O’Rahilly,et al.  The GPR54 gene as a regulator of puberty. , 2004, The New England journal of medicine.

[67]  A. Harmar,et al.  Transgenic approach reveals expression of the VPAC2 receptor in phenotypically defined neurons in the mouse suprachiasmatic nucleus and in its efferent target sites , 2004, The European journal of neuroscience.

[68]  F. Monsma,et al.  The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. , 2003, Biochemical and biophysical research communications.

[69]  S. O’Rahilly,et al.  The GPR54 Gene as a Regulator of Puberty , 2003 .

[70]  E. Génin,et al.  Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[71]  T. Kalamatianos,et al.  Studies on the Neuroanatomical Basis for Stress‐Induced Oestrogen‐Potentiated Suppression of Reproductive Function: Evidence Against Direct Corticotropin‐Releasing Hormone Projections to the Vicinity of Luteinizing Hormone‐Releasing Hormone Cell Bodies in Female Rats , 2003, Journal of neuroendocrinology.

[72]  Larry W Swanson,et al.  Structural characterization of a hypothalamic visceromotor pattern generator network , 2003, Brain Research Reviews.

[73]  B. Goldman,et al.  Perineal muscles and motoneurons are sexually monomorphic in the naked mole-rat (Heterocephalus glaber). , 2002, Journal of neurobiology.

[74]  S. Schiffmann,et al.  The Metastasis Suppressor Gene KiSS-1 Encodes Kisspeptins, the Natural Ligands of the Orphan G Protein-coupled Receptor GPR54* , 2001, The Journal of Biological Chemistry.

[75]  P. Emson,et al.  AXOR12, a Novel Human G Protein-coupled Receptor, Activated by the Peptide KiSS-1* , 2001, The Journal of Biological Chemistry.

[76]  E. Douzery,et al.  From the Old World to the New World: a molecular chronicle of the phylogeny and biogeography of hystricognath rodents. , 2001, Molecular phylogenetics and evolution.

[77]  O. Nishimura,et al.  Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor , 2001, Nature.

[78]  R. Magoul,et al.  The Gonadotropin‐Releasing Hormone Neurosecretory System of the Jerboa (Jaculus orientalis) and its Seasonal Variations , 2000, Journal of neuroendocrinology.

[79]  M. O'Riain,et al.  Morphological castes in a vertebrate. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[80]  L. Kriegsfeld,et al.  Photoperiod Affects the Gonadotropin- Releasing Hormone Neuronal System of Male Prairie Voles (Microtus ochrogaster) , 1999, Neuroendocrinology.

[81]  C. Sisk,et al.  Regional changes in GnRH immunoreactivity with puberty in the male Syrian hamster , 1999, Brain Research.

[82]  F. Clarke,et al.  Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole–rat, Heterocephalus glaber , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[83]  B. Rubin,et al.  Expression of Fos within luteinizing hormone-releasing hormone neurons, in relation to the steroid-induced luteinizing hormone surge in guinea pigs. , 1998, Biology of reproduction.

[84]  B. Rubin,et al.  Fos expression in luteinizing hormone-releasing hormone neurons of guinea pigs, with knife cuts separating the preoptic area and the hypothalamus, demonstrating luteinizing hormone surges. , 1998, Biology of reproduction.

[85]  J. Skinner,et al.  Distribution and morphology of luteinising hormone‐releasing hormone neurones in a species of wild antelope, the Springbok (Antidorcas marsupialis) , 1997, The Journal of comparative neurology.

[86]  J. Jarvis,et al.  Ecological constraints drive social evolution in the African mole–rats , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[87]  R W Guillery,et al.  Quantification without pontification: Choosing a method for counting objects in sectioned tissues , 1997, The Journal of comparative neurology.

[88]  F. Clarke,et al.  Dominance and queen succession in captive colonies of the eusocial naked mole–rat, Heterocephalus glaber , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[89]  C. G. Faulkes,et al.  Combined Olfactory Contact with the Parent Colony and Direct Contact with Nonbreeding Animals Does Not Maintain Suppression of Ovulation in Female Naked Mole-Rats (Heterocephalus glaber) , 1997, Hormones and Behavior.

[90]  J. Jarvis,et al.  Investigation of numbers and motility of spermatozoa in reproductively active and socially suppressed males of two eusocial African mole-rats, the naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Cryptomys damarensis). , 1994, Journal of reproduction and fertility.

[91]  J. Jarvis,et al.  Eusociality has evolved independently in two genera of bathyergid mole-rats — but occurs in no other subterranean mammal , 1993, Behavioral Ecology and Sociobiology.

[92]  C. G. Faulkes,et al.  Evidence that primer pheromones do not cause social suppression of reproduction in male and female naked mole-rats (Heterocephalus glaber). , 1993, Journal of reproduction and fertility.

[93]  J. Jarvis,et al.  LH responses to single doses of exogenous GnRH by freshly captured Damaraland mole-rats, Cryptomys damarensis. , 1993, Journal of reproduction and fertility.

[94]  P. Bateson,et al.  Measuring behaviour: Analysis and interpretation of data , 1993 .

[95]  L. Martinet,et al.  Gonadotropin-releasing hormone neurons and pathways in the brain of the female mink (Mustela vison) , 1992, Cell and Tissue Research.

[96]  C. G. Faulkes,et al.  Social control of reproduction in breeding and non-breeding male naked mole-rats (Heterocephalus glaber). , 1991, Journal of reproduction and fertility.

[97]  H. Urbanski,et al.  Immunocytochemical investigation of luteinizing hormone-releasing hormone neurons in Syrian hamsters maintained under long or short days. , 1991, Biology of reproduction.

[98]  H. Urbanski Monoclonal antibodies to luteinizing hormone-releasing hormone: production, characterization, and immunocytochemical application. , 1991, Biology of reproduction.

[99]  J. Jarvis,et al.  Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber. , 1991, Journal of reproduction and fertility.

[100]  J. Jarvis,et al.  LH responses of female naked mole-rats, Heterocephalus glaber, to single and multiple doses of exogenous GnRH. , 1990, Journal of reproduction and fertility.

[101]  J. Jarvis,et al.  Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber. , 1990, Journal of reproduction and fertility.

[102]  M. Lehman,et al.  The gonadotropin-releasing hormone neuronal system of the male Djungarian hamster: distribution from the olfactory tubercle to the medial basal hypothalamus. , 1990, Neuroendocrinology.

[103]  D. Pfaff,et al.  Origin of luteinizing hormone-releasing hormone neurons , 1989, Nature.

[104]  D. Pfaff,et al.  Immunocytochemical localization of luteinizing hormone‐releasing hormone (LHRH) in the brain and nervus terminalis of the adult and early neonatal gray short‐tailed opossum (Monodelphis domestica) , 1988, The Journal of comparative neurology.

[105]  J. Hodges,et al.  Social status controls LH secretion and ovulation in female marmoset monkeys (Callithrix jacchus). , 1988, The Journal of endocrinology.

[106]  Nigel C. Bennett,et al.  The Social Structure and Reproductive Biology of Colonies of the Mole-Rat, Cryptomys damarensis (Rodentia, Bathyergidae) , 1988 .

[107]  D. Zahniser,et al.  Changes in populations of LHRH-immunopositive cell bodies following gonadectomy , 1987, Peptides.

[108]  G. Hoffman,et al.  A developmental study of the quantitative distribution of LHRH neurons within the central nervous system of postnatal male and female rats , 1986, The Journal of comparative neurology.

[109]  J. Glass Short photoperiod-induced gonadal regression: effects on the gonadotropin-releasing hormone (GnRH) neuronal system of the white-footed mouse, Peromyscus leucopus. , 1986, Biology of reproduction.

[110]  M. Lehman,et al.  Immunocytochemical localization of luteinizing hormone‐releasing hormone (LHRH) pathways in the sheep brain during anestrus and the mid‐luteal phase of the estrous cycle , 1986, The Journal of comparative neurology.

[111]  J. C. King,et al.  LHRH neurons and their projections in humans and other mammals: Species comparisons , 1984, Peptides.

[112]  D. Gross The mammalian hypophysial pars tuberalis: a comparative immunocytochemical study. , 1984, General and comparative endocrinology.

[113]  E. Stopa,et al.  Immunocytochemical localization of LHRH in the median eminence, infundibular stalk, and neurohypophysis , 1984, Cell and Tissue Research.

[114]  J. A. Robinson,et al.  The luteinizing hormone‐releasing hormone pathways in rhesus (Macaca mulatta) and pigtailed (Macaca nemestrina) monkeys: New observations on thick, unembedded sections , 1982, The Journal of comparative neurology.

[115]  G. E. Huffman,et al.  LHRH pathways in rat brain: ‘Deafferentation’ spares a sub-chiasmatic LHRH projection to the median eminence , 1982, Neuroscience.

[116]  J. Witkin,et al.  The luteinizing hormone-releasing hormone (LHRH) systems in the rat brain. , 1982, Neuroendocrinology.

[117]  J. Jarvis Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. , 1981, Science.

[118]  A. Silverman Distribution of luteinizing hormone-releasing hormone (LHRH) in the guinea pig brain. , 1976, Endocrinology.

[119]  R. Goy,et al.  Progesterone concentrations in the arterial poasma of guinea-pigs during the oestrous cycle. , 1968, The Journal of endocrinology.

[120]  A. Herbison,et al.  Gonadotropin-releasing hormone (GnRH) neuron requirements for puberty, ovulation and fertility , 2018 .

[121]  A. Herbison CHAPTER 28 – Physiology of the Gonadotropin-Releasing Hormone Neuronal Network , 2006 .

[122]  J. D. Hahn,et al.  Comparative study of the sources of neuronal projections to the site of gonadotrophin‐releasing hormone perikarya and to the anteroventral periventricular nucleus in female rats , 2006, The Journal of comparative neurology.

[123]  P. Magni,et al.  Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. , 2005, Endocrinology.

[124]  R. Steiner,et al.  Behavioral / Systems / Cognitive Activation of Gonadotropin-Releasing Hormone Neurons by Kisspeptin as a Neuroendocrine Switch for the Onset of Puberty , 2005 .

[125]  W. Stumpf,et al.  LHRH-systems in the brain of the golden hamster , 2004, Cell and Tissue Research.

[126]  N. Bennett,et al.  A neuroanatomical and neuroendocrinological study into the relationship between social status and the GnRH system in cooperatively breeding female Damaraland mole-rats, Cryptomys damarensis. , 2004, Reproduction.

[127]  I. Merchenthaler,et al.  Gonadotropin-releasing hormone (GnRH) neurons and pathways in the rat brain , 2004, Cell and Tissue Research.

[128]  A. Janke,et al.  Molecular evidence of an African Phiomorpha-South American Caviomorpha clade and support for Hystricognathi based on the complete mitochondrial genome of the cane rat (Thryonomys swinderianus). , 2001, Molecular phylogenetics and evolution.

[129]  M. Jimenez-Linan,et al.  Examination of guinea pig luteinizing hormone-releasing hormone gene reveals a unique decapeptide and existence of two transcripts in the brain. , 1997, Endocrinology.

[130]  R. Coggeshall,et al.  Methods for determining numbers of cells and synapses: A case for more uniform standards of review , 1996, The Journal of comparative neurology.

[131]  C. Saper,et al.  Any way you cut it: A new journal policy for the use of unbiased counting methods , 1996, The Journal of comparative neurology.

[132]  R. Martínez-Rodríguez,et al.  Immunocytochemical localization of GnRH in the hypothalamus of the bat Miniopterus schreibersii schreibersii. , 1992, Journal fur Hirnforschung.

[133]  E. Stopa,et al.  Luteinizing hormone-releasing hormone neurons in human preoptic/hypothalamus: differential intraneuronal localization of immunoreactive forms. , 1985, The Journal of clinical endocrinology and metabolism.

[134]  D. Pfaff,et al.  Immunocytochemical localization of luteinizing hormone-releasing hormone in male and female rat brains. Quantitative studies on the effect of gonadal steroids. , 1983, Neuroendocrinology.

[135]  R. Gorski,et al.  Gonadotrophic hormone secretion in female rats after partial or total interruption of neural afferents to the medial basal hypothalamus. , 1967, Endocrinology.

[136]  J. T. Smith,et al.  A Role for Kisspeptins in the Regulation of Gonadotropin Secretion in the Mouse Materials and Methods Animals and Chemicals , 2022 .