Exogenous melatonin reproduces the effects of short day lengths on hippocampal function in male white-footed mice, Peromyscus leucopus

Neuroscience

Volumn 248, Issue , 2013, Pages 403-413

  Walton, J C ^a   Chen, Z ^b   Travers, J B ^b   Nelson, R J ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Barnes maze; Hippocampus; LTP; Melatonin; Neuronal morphology; Photoperiod

Indexed keywords

MELATONIN; DELAYED RELEASE FORMULATION; DRUG IMPLANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELL SIZE; CONTROLLED STUDY; DENDRITE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HORMONE RELEASE; HORMONE RESPONSE; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL; NONHUMAN; PEROMYSCUS; PHOTOPERIODICITY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPATIAL LEARNING; SPATIAL MEMORY; ANATOMY AND HISTOLOGY; ANIMAL; CYTOLOGY; DELAYED RELEASE FORMULATION; DRUG EFFECTS; DRUG IMPLANT; HIPPOCAMPUS; MAZE TEST; MEMORY; PHYSIOLOGY; SPATIAL BEHAVIOR;

ANIMALS; CA1 REGION, HIPPOCAMPAL; DELAYED-ACTION PREPARATIONS; DENDRITES; DRUG IMPLANTS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MELATONIN; MEMORY; MICE; NEURONS; PEROMYSCUS; PHOTOPERIOD; SPATIAL BEHAVIOR;

EID: 84880954215     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.06.020     Document Type: Article

References (53)

1. Bartness T.J., Powers J.B., Hastings M.H., Bittman E.L., Goldman B.D. The timed infusion paradigm for melatonin delivery: what has it taught us about the melatonin signal, its reception, and the photoperiodic control of seasonal responses?. J Pineal Res 1993, 15:161-190.
2. Bittman E.L., Karsch F.J. Nightly duration of pineal melatonin secretion determines the reproductive response to inhibitory day length in the ewe. Biol Reprod 1984, 30:585-593.
3. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
4. Bratton S.P. Resource division in an understory herb community - responses to temporal and microtopographic gradients. Am Nat 1976, 110:679-693.
5. Cao X.J., Wang M., Chen W.H., Zhu D.M., She J.Q., Ruan D.Y. Effects of chronic administration of melatonin on spatial learning ability and long-term potentiation in lead-exposed and control rats. Biomed Environ Sci 2009, 22:70-75.
6. Carlson L.L., Zimmermann A., Lynch G.R. Geographic differences for delay of sexual maturation in Peromyscus leucopus: effects of photoperiod, pinealectomy, and melatonin. Biol Reprod 1989, 41:1004-1013.
7. Carter D.S., Goldman B.D. Antigonadal effects of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): duration is the critical parameter. Endocrinology 1983, 113:1261-1267.
8. Collins D.R., Davies S.N. Melatonin blocks the induction of long-term potentiation in an N-methyl-d-aspartate independent manner. Brain Res 1997, 767:162-165.
9. Collinson N., Kuenzi F.M., Jarolimek W., Maubach K.A., Cothliff R., Sur C., Smith A., Otu F.M., Howell O., Atack J.R., McKernan R.M., Seabrook G.R., Dawson G.R., Whiting P.J., Rosahl T.W. Enhanced learning and memory and altered GABAergic synaptic transmission in mice lacking the alpha 5 subunit of the GABAA receptor. J Neurosci 2002, 22:5572-5580.
10. Cooke B.M., Woolley C.S. Gonadal hormone modulation of dendrites in the mammalian CNS. J Neurobiol 2005, 64:34-46.
11. Dark J., Zucker I., Wade G.N. Photoperiodic regulation of body mass, food intake, and reproduction in meadow voles. Am J Physiol 1983, 245:R334-R338.
12. Dowell S.F., Lynch G.R. Duration of the melatonin pulse in the hypothalamus controls testicular function in pinealectomized mice (Peromyscus leucopus). Biol Reprod 1987, 36:1095-1101.
13. El-Sherif Y., Hogan M.V., Tesoriero J., Wieraszko A. Factors regulating the influence of melatonin on hippocampal evoked potentials: comparative studies on different strains of mice. Brain Res 2002, 945:191-201.
14. Feng Y., Zhang L.X., Chao D.M. Role of melatonin in spatial learning and memory in rats and its mechanism. Sheng Li Xue Bao 2002, 54:65-70.
15. Fitch J.M., Juraska J.M., Washington L.W. The dendritic morphology of pyramidal neurons in the rat hippocampal CA3 area. I. Cell types. Brain Res 1989, 479:105-114.
16. Galea L.A., Kavaliers M., Ossenkopp K.P. Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J Exp Biol 1996, 199:195-200.
17. Galea L.A., Kavaliers M., Ossenkopp K.P., Innes D., Hargreaves E.L. Sexually dimorphic spatial learning varies seasonally in two populations of deer mice. Brain Res 1994, 635:18-26.
18. Golombek D.A., Pevet P., Cardinali D.P. Melatonin effects on behavior: possible mediation by the central GABAergic system. Neurosci Biobehav Rev 1996, 20:403-412.
19. Gupta R.R., Sen S., Diepenhorst L.L., Rudick C.N., Maren S. Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats(1). Brain Res 2001, 888:356-365.
20. Harley C.W., Malsbury C.W., Squires A., Brown R.A. Testosterone decreases CA1 plasticity in vivo in gonadectomized male rats. Hippocampus 2000, 10:693-697.
21. Hebbard P.C., King R.R., Malsbury C.W., Harley C.W. Two organizational effects of pubertal testosterone in male rats: transient social memory and a shift away from long-term potentiation following a tetanus in hippocampal CA1. Exp Neurol 2003, 182:470-475.
22. Institute of Laboratory Animal Resources (U.S.) Guide for the care and use of laboratory animals 1996, National Academy Press, Washington, DC.
23. Jacobs L.F. The economy of winter: phenotypic plasticity in behavior and brain structure. Biol Bull 1996, 191:92-100.
24. Johnston P.G., Zucker I. Antigonadal effects of melatonin in white-footed mice (Peromyscus leucopus). Biol Reprod 1980, 23:1069-1074.
25. Kanterewicz B.I., Golombek D.A., Rosenstein R.E., Cardinali D.P. Diurnal changes of GABA turnover rate in brain and pineal gland of Syrian hamsters. Brain Res Bull 1993, 31:661-666.
26. Kanterewicz B.I., Rosenstein R.E., Golombek D.A., Yannielli P.C., Cardinali D.P. Daily variations in GABA receptor function in Syrian hamster cerebral cortex. Neurosci Lett 1995, 200:211-213.
27. King J.A. Biology of Peromyscus (Rodentia) 1968, American Society of Mammalogist, Stillwater, Okla.
28. Leranth C., Petnehazy O., MacLusky N.J. Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J Neurosci 2003, 23:1588-1592.
29. Malpaux B., Migaud M., Tricoire H., Chemineau P. Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. J Biol Rhythms 2001, 16:336-347.
30. Nelson R.J., Denlinger D.L., Somers D.E. Photoperiodism: the biological calendar 2010, Oxford University Press, Oxford, New York.
31. Niles L.P., Pickering D.S., Arciszewski M.A. Effects of chronic melatonin administration on GABA and diazepam binding in rat brain. J Neural Transm 1987, 70:117-124.
32. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2004, Elsevier Academic Press, Amsterdam, Boston.
33. Petterborg L.J., Reiter R.J. Effect of photoperiod and melatonin on testicular development in the white-footed mouse, Peromyscus leucopus. J Reprod Fertil 1980, 60:209-212.
34. Popov V.I., Bocharova L.S., Bragin A.G. Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation. Neuroscience 1992, 48:45-51.
35. Pyter L.M., Reader B.F., Nelson R.J. Short photoperiods impair spatial learning and alter hippocampal dendritic morphology in adult male white-footed mice (Peromyscus leucopus). J Neurosci 2005, 25:4521-4526.
36. Pyter L.M., Trainor B.C., Nelson R.J. Testosterone and photoperiod interact to affect spatial learning and memory in adult male white-footed mice (Peromyscus leucopus). Eur J Neurosci 2006, 23:3056-3062.
37. Reiter R.J. The melatonin rhythm: both a clock and a calendar. Experientia 1993, 49:654-664.
38. Reiter R.J., Tan D.X., Fuentes-Broto L. Melatonin: a multitasking molecule. Prog Brain Res 2010, 181:127-151.
39. Rosenstein R.E., Cardinali D.P. Melatonin increases in vivo GABA accumulation in rat hypothalamus, cerebellum, cerebral cortex and pineal gland. Brain Res 1986, 398:403-406.
40. Schummers J., Browning M.D. Evidence for a role for GABA(A) and NMDA receptors in ethanol inhibition of long-term potentiation. Brain Res Mol Brain Res 2001, 94:9-14.
41. Skuckas V.A., Duffy A.M., Harte-Hargrove L.C., Magagna-Poveda A., Radman T., Chakraborty G., Schroeder C.E., MacLusky N.J., Scharfman H.E. Testosterone depletion in adult male rats increases mossy fiber transmission, LTP, and sprouting in area CA3 of hippocampus. J Neurosci 2013, 33:2338-2355.
42. Talaei S.A., Sheibani V., Salami M. Light deprivation improves melatonin related suppression of hippocampal plasticity. Hippocampus 2010, 20:447-455.
43. Tamarkin L., Hollister C.W., Lefebvre N.G., Goldman B.D. Melatonin induction of gonadal quiescence in pinealectomized Syrian hamsters. Science 1977, 198:953-955.
44. Turek F.W., Desjardins C., Menaker M. Melatonin-induced inhibition of testicular function in adult golden hamsters. Proc Soc Exp Biol Med 1976, 151:502-506.
45. Walton J.C., Chen Z., Weil Z.M., Pyter L.M., Travers J.B., Nelson R.J. Photoperiod-mediated impairment of long-term potentiation and learning and memory in male white-footed mice. Neuroscience 2011, 175:127-132.
46. Walton J.C., Haim A., Spieldenner J.M., Nelson R.J. Photoperiod alters fear responses and basolateral amygdala neuronal spine density in white-footed mice (Peromyscus leucopus). Behav Brain Res 2012, 233:345-350.
47. Walton J.C., Pyter L.M., Weil Z.M., Nelson R.J. Photoperiod mediated changes in olfactory bulb neurogenesis and olfactory behavior in male white-footed mice (Peromyscus leucopus). PLoS One 2012, 7:e42743.
48. Walton J.C., Weil Z.M., Nelson R.J. Influence of photoperiod on hormones, behavior, and immune function. Front Neuroendocrinol 2011, 32:303-319.
49. Wang L.M., Suthana N.A., Chaudhury D., Weaver D.R., Colwell C.S. Melatonin inhibits hippocampal long-term potentiation. Eur J Neurosci 2005, 22:2231-2237.
50. Workman J.L., Bowers S.L., Nelson R.J. Enrichment and photoperiod interact to affect spatial learning and hippocampal dendritic morphology in white-footed mice (Peromyscus leucopus). Eur J Neurosci 2009, 29:161-170.
51. Workman J.L., Manny N., Walton J.C., Nelson R.J. Short day lengths alter stress and depressive-like responses, and hippocampal morphology in Siberian hamsters. Horm Behav 2011, 60:520-528.
52. Yaskin V.A. Seasonal changes in hippocampus size and spatial behaviour in mammals and birds. Zh Obshch Biol 2011, 72:27-39.
53. Yellon S.M., Tamarkin L., Pratt B.L., Goldman B.D. Pineal melatonin in the Djungarian hamster: photoperiodic regulation of a circadian rhythm. Endocrinology 1982, 111:488-492.