Receipt of vaginal-cervical stimulation modifies synapsin content in limbic areas of the female rat

Neuroscience

Volumn 153, Issue 3, 2008, Pages 581-593

  Oberlander, J G ^a   Erskine, M S ^a  

^a Boston University   (United States)

Author keywords

BLA; hippocampus; medial amygdala; memory; pseudopregnancy; synaptic paring

Indexed keywords

SYNAPSIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN DEPTH STIMULATION; CONFOCAL MICROSCOPY; CONTROL GROUP; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LIMBIC CORTEX; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; VASECTOMY;

EID: 43049110184     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.02.048     Document Type: Article

References (82)

1. J.E. Black K.R. Isaacs B.J. Anderson A.A. Alcantara W.T. Greenough Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats Proc Natl Acad Sci U S A 87 1990 5568 5572
2. J. Bock K. Braun Differential emotional experience leads to pruning of dendritic spines in the forebrain of domestic chicks Neural Plast 6 1998 17 27
3. J. Bock K. Braun Blockade of N-methyl-D-aspartate receptor activation suppresses learning-induced synaptic elimination Proc Natl Acad Sci U S A 96 1999 2485 2490
4. J. Bock K. Braun Filial imprinting in domestic chicks is associated with spine pruning in the associative area, dorsocaudal neostriatum Eur J Neurosci 11 1999 2566 2570
5. N.M. Cameron P. Carey M.S. Erskine Medullary noradrenergic neurons release norepinephrine in the medial amygdala in females in response to mating stimulation sufficient for pseudopregnancy Brain Res 1022 2004 137 147
6. P. Chi P. Greengard T.A. Ryan Synapsin dispersion and reclustering during synaptic activity Nat Neurosci 4 2001 1187 1193
7. R.L. Cooper J.M. Goldman J.G. Vandenbergh Monitoring of the estrous cycle in the laboratory rodent by vaginal lavage J.J. Heindel R.E. Chapin Methods in toxicology Vol. 3 1993 Academic Press, Inc New York 45 55
8. C. Coopersmith S.E. Gans D.W. Rowe M.S. Erskine Infusions of lidocaine into the amygdala, but not the preoptic area, block pseudopregnancy in the rat J Neuroendocrinol 8 1996 259 266
9. N. Dafny J. Terkel Hypothalamic neuronal activity associated with onset of pseudopregnancy in the rat Neuroendocrinology 51 1990 459 467
10. W.J. De Greef G.H. Zeilmaker Prolactin and delayed pseudopregnancy in the rat Endocrinology 98 1976 305 310
11. M. Diamond Intromission pattern and species vaginal code in relation to induction of pseudopregnancy Science 169 1970 995 997
12. M. Dragunow A role for immediate-early transcription factors in learning and memory Behav Genet 26 1996 293 299
13. M.S. Erskine Mating-induced increases in FOS protein in preoptic area and medial amygdala of cycling female rats Brain Res Bull 32 1993 447 451
14. M.S. Erskine Prolactin release after mating and genitosensory stimulation in females Endocr Rev 16 1995 508 528
15. M.S. Erskine S.B. Hanrahan Effects of paced mating on c-fos gene expression in the female rat brain J Neuroendocrinol 9 1997 903 912
16. M.S. Erskine E. Kornberg J.A. Cherry Paced copulation in rats: effects of intromission frequency and duration on luteal activation and estrus length Physiol Behav 45 1989 33 39
17. M.S. Erskine M.L. Lehmann N.M. Cameron E.K. Polston Co-regulation of female sexual behavior and pregnancy induction: an exploratory synthesis Behav Brain Res 153 2004 295 315
18. J.W. Everett D.L. Quinn Differential hypothalamic mechanisms inciting ovulation and pseudopregnancy in the rat Endocrinology 78 1966 141 150
19. T.L. Fletcher P. Cameron P. De Camilli G. Banker The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture J Neurosci 11 1991 1617 1626
20. Y. Geinisman Structural synaptic modifications associated with hippocampal LTP and behavioral learning Cereb Cortex 10 2000 952 962
21. Y. Geinisman R.W. Berry J.F. Disterhoft J.M. Power E.A. Van der Zee Associative learning elicits the formation of multiple-synapse boutons J Neurosci 21 2001 5568 5573
22. D.P. Gilman L.F. Mercer J.C. Hitt Influence of female copulatory behavior on the induction of pseudopregnancy in the female rat Physiol Behav 22 1979 675 678
23. B. Granseth E. Ahlstrand S. Lindstrom Paired pulse facilitation of corticogeniculate EPSCs in the dorsal lateral geniculate nucleus of the rat investigated in vitro J Physiol 544 2002 477 486
24. P. Greengard F. Benfenati F. Valtorta Synapsin I, an actin-binding protein regulating synaptic vesicle traffic in the nerve terminal Adv Second Messenger Phosphoprotein Res 29 1994 31 45
25. P. Greengard F. Valtorta A.J. Czernik F. Benfenati Synaptic vesicle phosphoproteins and regulation of synaptic function Science 259 1993 780 785
26. D.F. Hardy J.F. DeBold Effects of coital stimulation upon behavior of the female rat J Comp Physiol Psychol 78 1972 400 408
27. S. Hilfiker V.A. Pieribone A.J. Czernik H.T. Kao G.J. Augustine P. Greengard Synapsins as regulators of neurotransmitter release Philos Trans R Soc Lond B Biol Sci 354 1999 269 279
28. F.W. Hopf J. Waters S. Mehta S.J. Smith Stability and plasticity of developing synapses in hippocampal neuronal cultures J Neurosci 22 2002 775 781
29. M. Kawakami K. Kubo Neuro-correlate of limbic-hypothalamo-pituitary-gonadal axis in the rat: change in limbic-hypothalamic unit activity induced by vaginal and electrical stimulation Neuroendocrinology 7 1971 65 89
30. A. Kielland A. Erisir S.I. Walaas P. Heggelund Synapsin utilization differs among functional classes of synapses on thalamocortical cells J Neurosci 26 2006 5786 5793
31. J.A. Kleim J.H. Freeman Jr R. Bruneau B.C. Nolan N.R. Cooper A. Zook D. Walters Synapse formation is associated with memory storage in the cerebellum Proc Natl Acad Sci U S A 99 2002 13228 13231
32. S. Knafo F. Libersat E. Barkai Olfactory learning-induced morphological modifications in single dendritic spines of young rats Eur J Neurosci 21 2005 2217 2226
33. J.J. Knierim Neural representations of location outside the hippocampus Learn Mem 13 2006 405 415
34. E. Kornberg M.S. Erskine Effects of differential mating stimulation on the onset of prolactin surges in pseudopregnant rats Psychoneuroendocrinology 19 1994 357 371
35. J.W. Lee M.S. Erskine Pseudorabies virus tracing of neural pathways between the uterine cervix and CNS: effects of survival time, estrogen treatment, rhizotomy, and pelvic nerve transection J Comp Neurol 418 2000 484 503
36. M.L. Lehmann M.S. Erskine Induction of pseudopregnancy using artificial VCS: importance of lordosis intensity and prestimulus estrous cycle length Horm Behav 45 2004 75 83
37. M.L. Lehmann M.S. Erskine Glutamatergic stimulation of the medial amygdala induces steroid dependent c-fos expression within forebrain nuclei responsive to mating stimulation Neuroscience 136 2005 55 64
38. M.L. Lehmann H. McKellar M.S. Erskine Coding for the initiation of pseudopregnancy by temporally patterned activation of amygdalar NMDA receptors J Neurosci 25 2005 8696 8703
39. L. Li L.S. Chin O. Shupliakov L. Brodin T.S. Sihra O. Hvalby V. Jensen D. Zheng J.O. McNamara P. Greengard Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice Proc Natl Acad Sci U S A 92 1995 9235 9239
40. R. Llinas T.L. McGuinness C.S. Leonard M. Sugimori P. Greengard Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse Proc Natl Acad Sci U S A 82 1985 3035 3039
41. B. Lu P. Greengard M.M. Poo Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses Neuron 8 1992 521 529
42. M.A. Lynch K.L. Voss J. Rodriguez T.V. Bliss Increase in synaptic vesicle proteins accompanies long-term potentiation in the dentate gyrus Neuroscience 60 1994 1 5
43. G.W. Mathern E.H. Bertram 3rd T.L. Babb J.K. Pretorius P.A. Kuhlman S. Spradlin D. Mendoza In contrast to kindled seizures, the frequency of spontaneous epilepsy in the limbic status model correlates with greater aberrant fascia dentata excitatory and inhibitory axon sprouting, and increased staining for N-methyl-D-aspartate, AMPA and GABA(A) receptors Neuroscience 77 1997 1003 1019
44. N. Matus-Leibovitch V. Ezra-Macabee D. Saya B. Attali T. Avidor-Reiss J. Barg Z. Vogel Increased expression of synapsin I mRNA in defined areas of the rat central nervous system following chronic morphine treatment Brain Res Mol Brain Res 34 1995 221 230
45. 14C]2-deoxyglucose uptake in female rat brain produced by electrical stimulation of hypothalamic and limbic brain areas Neuroscience 24 1988 241 263
46. R.H. Melloni Jr L.J. DeGennaro Temporal onset of synapsin I gene expression coincides with neuronal differentiation during the development of the nervous system J Comp Neurol 342 1994 449 462
47. R. Miranda E. Blanco A. Begega L.J. Santin J.L. Arias Reversible changes in hippocampal CA1 synapses associated with water maze training in rats Synapse 59 2006 177 181
48. S. Miyoshi M. Okada Storage capacity diverges with synaptic efficiency in an associative memory model with synaptic delay and pruning IEEE Trans Neural Netw 15 2004 1215 1227
49. M. Mokin J. Keifer Quantitative analysis of immunofluorescent punctate staining of synaptically localized proteins using confocal microscopy and stereology J Neurosci Methods 157 2006 218 224
50. R.Y. Moore M.E. Bernstein Synaptogenesis in the rat suprachiasmatic nucleus demonstrated by electron microscopy and synapsin I immunoreactivity J Neurosci 9 1989 2151 2162
51. K. Morimoto K. Sato S. Sato N. Yamada T. Hayabara Time-dependent changes in rat hippocampal synapsin I mRNA expression during long-term potentiation Brain Res 783 1998 57 62
52. E.J. Nestler T.C. Rainbow B.S. McEwen P. Greengard Corticosterone increases the amount of protein 1, a neuron-specific phosphoprotein, in rat hippocampus Science 212 1981 1162 1164
53. A.M. Nikolakopoulou H.A. Davies M.G. Stewart Passive avoidance training decreases synapse density in the hippocampus of the domestic chick Eur J Neurosci 23 2006 1054 1062
54. L.E. Northrop J.L. Shadrach M.S. Erskine Noradrenergic innervation of the ventromedial hypothalamus is involved in mating-induced pseudopregnancy in the female rat J Neuroendocrinol 18 2006 577 583
55. Oberlander JG, Yang JJ, Erskine MS (2007) Differential mating stimulation decreases synapsin punctae and increases synapsin intensity in limbic neurons of female rat. In: Society for Neuroscience, Poster 295.220, San Diego.
56. K.D. Parfitt B.J. Hoffer M.D. Browning Norepinephrine and isoproterenol increase the phosphorylation of synapsin I and synapsin II in dentate slices of young but not aged Fisher 344 rats Proc Natl Acad Sci U S A 88 1991 2361 2365
57. G. Paxinos C. Watson The rat brain in stereotaxic coordinates 1998 Academic Press San Diego, CA
58. J.G. Pfaus M.M. Heeb Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents Brain Res Bull 44 1997 397 407
59. J.G. Pfaus S.P. Kleopoulos C.V. Mobbs R.B. Gibbs D.W. Pfaff Sexual stimulation activates c-fos within estrogen-concentrating regions of the female rat forebrain Brain Res 624 1993 253 267
60. E.K. Polston M.S. Erskine Patterns of induction of the immediate-early genes c-fos and egr-1 in the female rat brain following differential amounts of mating stimulation Neuroendocrinology 62 1995 370 384
61. E.K. Polston M.S. Erskine Excitotoxic lesions of the medial amygdala differentially disrupt prolactin secretory responses in cycling and mated female rats J Neuroendocrinol 13 2001 13 21
62. E.K. Polston M. Heitz W. Barnes K. Cardamone M.S. Erskine NMDA-mediated activation of the medial amygdala initiates a downstream neuroendocrine memory responsible for pseudopregnancy in the female rat J Neurosci 21 2001 4104 4110
63. T.C. Rainbow B. Parsons N.J. MacLusky B.S. McEwen Estradiol receptor levels in rat hypothalamic and limbic nuclei J Neurosci 2 1982 1439 1445
64. A.A. Rasia-Filho C. Fabian K.M. Rigoti M. Achaval Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method Neuroscience 126 2004 839 847
65. S.P. Rose M.G. Stewart Cellular correlates of stages of memory formation in the chick following passive avoidance training Behav Brain Res 98 1999 237 243
66. D.W. Rowe M.S. Erskine c-Fos proto-oncogene activity induced by mating in the preoptic area, hypothalamus and amygdala in the female rat: role of afferent input via the pelvic nerve Brain Res 621 1993 25 34
67. J. Sambrook D.W. Russel Molecular cloning: a laboratory manual 2001 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
68. K. Sato K. Morimoto S. Suemaru T. Sato N. Yamada Increased synapsin I immunoreactivity during long-term potentiation in rat hippocampus Brain Res 872 2000 219 222
69. M. Segal Dendritic spines and long-term plasticity Nat Rev Neurosci 6 2005 277 284
70. T.J. Shors Memory traces of trace memories: neurogenesis, synaptogenesis and awareness Trends Neurosci 27 2004 250 256
71. S. Suemaru K. Sato K. Morimoto N. Yamada T. Sato S. Kuroda Increment of synapsin I immunoreactivity in the hippocampus of the rat kindling model of epilepsy Neuroreport 11 2000 1319 1322
72. 2+/calmodulin-dependent pathway Proc Natl Acad Sci U S A 103 2006 2880 2885
73. M. Tanaka M. Yoshida H. Emoto H. Ishii Noradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies Eur J Pharmacol 405 2000 397 406
74. J. Terkel J.A. Witcher N.T. Adler Evidence for “memory” of cervical stimulation for the promotion of pregnancy in rats Horm Behav 24 1990 40 49
75. M.J. Tetel M.J. Getzinger J.D. Blaustein Fos expression in the rat brain following vaginal-cervical stimulation by mating and manual probing J Neuroendocrinol 5 1993 397 404
76. B. Ullrich T.C. Sudhof Differential distributions of novel synaptotagmins: comparison to synapsins Neuropharmacology 34 1995 1371 1377
77. C.L. Waites A.M. Craig C.C. Garner Mechanisms of vertebrate synaptogenesis Annu Rev Neurosci 28 2005 251 274
78. H. Wang V.M. Pickel Activity-regulated cytoskeleton-associated protein Arc is targeted to dendrites and coexpressed with mu-opioid receptors in postnatal rat caudate-putamen nucleus J Neurosci Res 77 2004 323 333
79. P. Washbourne J.E. Bennett A.K. McAllister Rapid recruitment of NMDA receptor transport packets to nascent synapses Nat Neurosci 5 2002 751 759
80. R. Welschen P. Osman J. Dullaart W.J. de Greef J.T. Uilenbroek F.H. de Jong Levels of follicle-stimulating hormone, luteinizing hormone, oestradiol-17 beta and progesterone, and follicular growth in the pseudopregnant rat J Endocrinol 64 1975 37 47
81. C.S. Woolley B.S. McEwen Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism J Neurosci 14 1994 7680 7687
82. J.J. Yang J.G. Oberlander M.S. Erskine Expression of FOS, EGR-1, and ARC in the amygdala and hippocampus of female rats during formation of the intromission mnemonic of pseudopregnancy Dev Neurobiol 67 2007 895 908