Mating Increases Neuronal Tyrosine Hydroxylase Expression and Selectively Gates Transmission of Male Chemosensory Information in Female Mice

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Matthews, Gillian A ^a   Patel, Ronak ^a   Walsh, Alison ^a   Davies, Owain ^a   Martínez Ricós, Joana ^b   Brennan, Peter A ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; PROTEIN C FOS; TYROSINE 3 MONOOXYGENASE;

ACCESSORY OLFACTORY BULB; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BAGG ALBINO MOUSE; BRAIN DEPTH STIMULATION; C57BL 6 MOUSE; CELL COUNT; CONTROLLED STUDY; CORTICOMEDIAL AMYGDALA; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; FEMALE; MALE; MATING; MOUSE; NEUROMODULATION; NONHUMAN; OLFACTORY BULB; PREGNANCY TERMINATION; PREIMPLANTATION EMBRYO; PROTEIN EXPRESSION; SENSORY NERVE CELL; SENSORY NERVE CONDUCTION; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; VOMERONASAL ORGAN;

AMYGDALA; ANIMALS; ARCUATE NUCLEUS; DOPAMINE; EMBRYO IMPLANTATION; FEMALE; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEURONS; OLFACTORY BULB; PHEROMONES; PREGNANCY; PROTO-ONCOGENE PROTEINS C-FOS; SEXUAL BEHAVIOR, ANIMAL; SYNAPTIC TRANSMISSION; TYROSINE 3-MONOOXYGENASE; VOMERONASAL ORGAN;

EID: 84880796205     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069943     Document Type: Article

References (32)

1. Brennan P, Kaba H, Keverne EB, (1990) Olfactory Recognition: a simple memory system. Science 250: 1223-1226. doi:10.1126/science.2147078. PubMed: 2147078.
2. Bruce HM, (1961) Time relations in the pregnancy-block induced in mice by strange males. J Reprod Fert 2: 138-142. doi:10.1530/jrf.0.0020138.
3. Li CS, Kaba H, Saito H, Seto K, (1989) Excitatory influence of the accessory olfactory bulb on tuberoinfundibular arcuate neurons of female mice and its modulation by oestrogen. Neuroscience 29: 201-208. doi:10.1016/0306-4522(89)90343-6. PubMed: 2710344.
4. Rosser AE, Remfry CJ, Keverne EB, (1989) Restricted exposure of mice to primer pheromones coincident with prolactin surges blocks pregnancy by changing hypothalamic dopamine release. J Reprod Fertil 87: 553-559. doi:10.1530/jrf.0.0870553. PubMed: 2513390.
5. Li CS, Kaba H, Seto K, (1994) Effective induction of pregnancy block by electrical stimulation of the mouse accessory olfactory bulb coincident with prolactin surges. Neurosci Lett 176: 5-8. doi:10.1016/0304-3940(94)90857-5. PubMed: 7970236.
6. Binns KE, Brennan PA, (2005) Changes in electrophysiological activity in the accessory olfactory bulb and medial amygdala associated with mate recognition in mice. Eur J Neurosci 21: 2529-2537. doi:10.1111/j.1460-9568.2005.04090.x. PubMed: 15932610.
7. Halem HA, Cherry JA, Baum MJ, (2001) Central forebrain Fos responses to familiar male odours are attenuated in recently mated female mice. Eur J Neurosci 13: 389-399. doi:10.1111/j.1460-9568.2001.01382.x. PubMed: 11168544.
8. Serguera C, Triaca V, Kelly-Barrett J, Banchaabouchi MA, Minichiello L, (2008) Increased dopamine after mating impairs olfaction and prevents odor interference with pregnancy. Nat Neurosci 11: 949-956. doi:10.1038/nn.2154. PubMed: 18641644.
9. Baker H, (1986) Species differences in the distribution of substance P and tyrosine hydroxylase immunoreactivity in the olfactory bulb. J Comp Neurol 252: 206-226. doi:10.1002/cne.902520206. PubMed: 2431012.
10. Rosser AE, Hökfelt T, Goldstein M, (1986) LHRH and catecholamine neuronal systems in the olfactory bulb of the mouse. J Comp Neurol 250: 352-363. doi:10.1002/cne.902500308. PubMed: 2875086.
11. Brennan PA, Hancock D, Keverne EB, (1992) The expression of the immediate-early genes c-fos, egr-1 and c-jun in the accessory olfactory bulb during the formation of an olfactory memory in mice. Neuroscience 49: 277-284. doi:10.1016/0306-4522(92)90095-J. PubMed: 1279452.
12. Abràmoff M, Magalhaes P, Ram S, (2004) Image processing with ImageJ. Biophotonics Int 11: 36-42.
13. Paxinos G, Franklin KBJ, (2001) The mouse brain in stereotaxic coordinates 2nd edition. San Diego: Academic Press.
14. Arbogast LA, Voogt JL, (1993) Progesterone reverses the estradiol-induced decrease in tyrosine hydroxylase mRNA levels in the arcuate nucleus. Neuroendocrinology 58: 501-510. doi:10.1159/000126583. PubMed: 7906870.
15. Arbogast LA, Voogt JL, (1991) Hyperprolactinemia increases and hypoprolactinemia decreases tyrosine hydroxylase messenger ribonucleic acid levels in the arcuate nuclei, but not the substantia nigra or zona incerta. Endocrinology 128: 997-1005. doi:10.1210/endo-128-2-997. PubMed: 1703487.
16. Barkley MS, Bradford GE, Geschwind II, (1978) The pattern of plasma prolactin concentration during the first half of mouse gestation. Biol Reprod 19: 291-296. doi:10.1095/biolreprod19.2.291. PubMed: 568955.
17. Lerant A, Herman ME, Freeman ME, (1996) Dopaminergic neurons of periventricular and arcuate nuclei of pseudopregnant rats: semicircadian rhythm in Fos-related antigens immunoreactivities and in dopamine concentration. Endocrinology 137: 3621-3628. doi:10.1210/en.137.9.3621. PubMed: 8756525.
18. Lloyd-Thomas A, Keverne EB, (1982) Role of the brain and accessory olfactory system in the block to pregnancy in mice. Neuroscience 7: 907-913. doi:10.1016/0306-4522(82)90051-3. PubMed: 7099424.
19. Ma D, Allen ND, Van Bergen YC, Jones CM, Baum MJ, et al. (2002) Selective ablation of olfactory receptor neurons without functional impairment of vomeronasal receptor neurons in OMP-ntr transgenic mice. Eur J Neurosci 16: 2317-2323. doi:10.1046/j.1460-9568.2002.02303.x. PubMed: 12492426.
20. Choi GB, Dong HW, Murphy AJ, Valenzuela DM, Yancopoulos GD, et al. (2005) Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46: 647-660. doi:10.1016/j.neuron.2005.04.011. PubMed: 15944132.
21. Samuelsen CL, Meredith M, (2009) Categorization of biologically relevant chemical signals in the medial amygdala. Brain Res 1263: 33-42. doi:10.1016/j.brainres.2009.01.048. PubMed: 19368822.
22. Hoppe PC, (1975) Genetic and endocrine studies of the pregnancy-blocking pheromone of mice. J Reprod Fertil 45: 109-115. doi:10.1530/jrf.0.0450109. PubMed: 127839.
23. Leinders-Zufall T, Brennan P, Widmayer P, Chandramani PS, Maul-Pavicic A, et al. (2004) MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306: 1033-1037. doi:10.1126/science.1102818. PubMed: 15528444.
24. Baker H, Liu N, Chun HS, Saino S, Berlin R, et al. (2001) Phenotypic differentiation during migration of dopaminergic progenitor cells to the olfactory bulb. J Neurosci 21: 8505-8513. PubMed: 11606639.
25. Baker H, Kawano T, Margolis FL, Joh TH, (1983) Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3: 69-78. PubMed: 6130133.
26. Hsia AY, Vincent JD, Lledo PM, (1999) Dopamine depresses synaptic inputs into the olfactory bulb. J Neurophysiol 82: 1082-1085. PubMed: 10444702.
27. Nara K, Saraiva LR, Ye X, Buck LB, (2011) A large-scale analysis of odor coding in the olfactory epithelium. J Neurosci 31: 9179-9191. doi:10.1523/JNEUROSCI.1282-11.2011. PubMed: 21697369.
28. Kimoto H, Haga S, Sato K, Touhara K, (2005) Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437: 898-901. doi:10.1038/nature04033. PubMed: 16208374.
29. Schaefer ML, Young DA, Restrepo D, (2001) Olfactory fingerprints for major histocompatibility complex-determined body odors. J Neurosci 21: 2481-2487. PubMed: 11264322.
30. Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, et al. (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405: 792-796. doi:10.1038/35015572. PubMed: 10866200.
31. Yokosuka M, (2012) Histological properties of the glomerular layer in the mouse accessory olfactory bulb. Exp Anim 61: 13-24. doi:10.1538/expanim.61.13. PubMed: 22293668.
32. Baker H, Joh TH, Ruggiero DA, Reis DJ, (1983) Variations in number of dopamine neurons and tyrosine hydroxylase activity in hypothalamus of two mouse strains. J Neurosci 3: 832-843. PubMed: 6131950.