Cell-body lesions of the posterodorsal preoptic nucleus or posterodorsal medial amygdala, but not the parvicellular subparafascicular thalamus, disrupt mating in male gerbils

Physiology and Behavior

Volumn 68, Issue 3, 2000, Pages 317-331

  Heeb, Michaela M ^a   Yahr, Pauline ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ejaculation; Male sex behavior, Medial amygdala; Medial preoptic area; Parvicellular part of subparafascicular nucleus of thalamus; Posterodorsal preoptic area

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EJACULATION; FEMALE; GERBIL; MALE; MATING; NEUROPSYCHOLOGY; NONHUMAN; PREOPTIC NUCLEUS; PRIORITY JOURNAL; THALAMUS;

EID: 0033984460     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0031-9384(99)00182-1     Document Type: Article

References (80)

1. Meisel R.L., Sachs B.D. The physiology of male sexual behavior. Knobil E., Neill J.D. The Physiology of Reproduction, vol 2. 2nd ed:1994;3-105 Raven Press, New York.
2. Pfaus J.G., Heeb M.M. Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Behav Brain Res. 44:1997;397-407.
3. Heeb M.M., Yahr P. C-fos immunoreactivity in the sexually dimorphic area of the hypothalamus and related brain regions of male gerbils after exposure to sex-related stimuli or performance of specific sexual behaviors. Neuroscience. 72:1996;1049-1071.
4. Baum M.J., Everitt B.J. Increased expression of c-fos in the medial preoptic area after mating in male rats. role of afferent inputs from the medial amygdala and midbrain central tegmental field Neuroscience. 50:1992;627-646.
5. Coolen L.M., Peters H.J.P.W., Veening J.G. Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior. a sex comparison Brain Res. 738:1996;67-82.
6. Robinson B.W., Mishkin M. Ejaculation evoked by stimulation of the preoptic area in monkey. Physiol Behav. 1:1966;269-272.
7. Arendash G.W., Gorski R.A. Effects of discrete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats. Brain Res Bull. 10:1983;147-154.
8. Emery D.E., Sachs B.D. Copulatory behavior in male rats with lesions in the bed nucleus of the stria terminalis. Physiol Behav. 17:1976;803-806.
9. Coolen L.M., Peters H.J.P.W., Veening J.G. Distribution of Fos immunoreactivity following mating versus anogenital investigation in the male rat brain. Neuroscience. 4:1997;1151-1161.
10. Fernandez-Fewell G.D., Meredith M. C-fos expression in vomeronasal pathways of mated or pheromone-stimulated male golden hamsters. contributions from vomeronasal sensory input and expression related to mating performance J Neurosci. 14:1994;3643-3654.
11. Kollack-Walker S.S., Newman S.W. Mating-induced expression of c-fos in the male Syrian hamster brain. role of experience, pheromones, and ejaculation J Neurobiol. 32:1997;481-501.
12. Parfitt D.B., Newman S.W. Fos-immunoreactivity within the extended amygdala is correlated with the onset of sexual satiety. Horm Behav. 34:1998;17-29.
13. Fiber J.M., Adames P., Swann J.M. Pheromones induce c-fos in limbic areas regulating male hamster mating behavior. Neuroreport. 4:1993;871-874.
14. Fiber J.M., Swann J.M. Testosterone differentially influences sex-specific pheromone-stimulated Fos expression in limbic regions of Syrian hamsters. Horm Behav. 30:1996;455-473.
15. Bakker J., Baum M.J., Slob A.K. Neonatal inhibition of estrogen synthesis alters adult neural Fos responses to mating and pheromonal stimulation in the male rat. Neuroscience. 74:1996;251-260.
16. Bressler S.C., Baum M.J. Sex comparison of neuronal Fos immunoreactivity in the rat vomeronasal projection circuit after chemosensory stimulation. Neuroscience. 71:1996;1063-1072.
17. Paredes R.G., Lopez M.E., Baum M.J. Testosterone augments neuronal Fos responses to estrous odors throughout the vomeronasal projection pathway of gonadectomized male and female rats. Horm Behav. 33:1998;48-57.
18. Lehman M.N., Powers J.B., Winans S.S. Stria terminalis lesions alter the temporal pattern of copulatory behavior in the male golden hamster. Behav Brain Res. 8:1983;109-128.
19. Lehman M.N., Winans S.S. Vomeronasal and olfactory pathways to the amygdala controlling male hamster sexual behavior. autoradiographic and behavioral studies Brain Res. 240:1982;27-41.
20. Lehman M.N., Winans S.S., Powers J.B. Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. Science. 210:1980;557-560.
21. DeJonge F.H., Oldenburger W.P., Louwerse Al Van De Poll N.E. Changes in male copulatory behavior after sexual exciting stimuli. effects of medial amygdala lesions Physiol Behav. 52:1992;327-332.
22. Kondo Y. Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats. Physiol Behav. 51:1992;939-943.
23. Kondo Y., Sachs B.D., Sakuma Y. Importance of the medial amygdala in rat penile erection evoked by remote stimuli from estrous females. Behav Brain Res. 88:1997;153-160.
24. McGregor A., Herbert J. Differential effects of excitotoxic basolateral and corticomedial lesions of the amygdala on the behavioural and endocrine responses to either sexual or aggression-promoting stimuli in the male rat. Brain Res. 574:1992;9-20.
25. Tsutsui Y., Shinoda A., Kondo Y. Facilitation of copulatory behavior by pCPA treatments following stria terminalis transection but not medial amygdala lesion in the male rat. Physiol Behav. 56:1994;603-608.
26. Commins D., Yahr P. Adult testosterone levels influence the morphology of a sexually dimorphic area in the Mongolian gerbil brain. J Comp Neurol. 224:1984;132-140.
27. Faull R.L.M., Mehler W.R. Thalamus. Paxinos G. The Rat Nervous SystemVol. 1. 1st ed:1985;129-168 Academic Press; Orlando, FL.
28. 1A agonist 8-OH-DPAT. Physiol Behav. 62:1997;881-891.
29. Coolen L.M., Peters H.J.P.W., Veening J.G. Anatomical interrelationships of the medial preoptic area and other brain regions activated following male sexual behavior. a combined Fos and tract-tracing study J Comp Neurol. 397:1998;421-435.
30. Yahr P., Gregory J.E. The medial and lateral cell groups of the sexually dimorphic area of the gerbil hypothalamus are essential for male sex behavior and act via separate pathways. Brain Res. 631:1993;287-296.
31. Maillard C.-A., Edwards D.A. Excitotoxin lesions of the zona incerta/lateral tegmentum continuum. effects on male sexual behavior in rats Behav Brain Res. 46:1991;143-149.
32. Maillard-Gutekunst C.-A., Edwards D.A. Preoptic and subthalamic connections with the caudal brainstem are important for copulation in the male rat. Behav Neurosci. 108:1994;758-766.
33. Hansen S., Kohler C. The importance of the peripeduncular nucleus in the neuroendocrine control of sexual behavior and milk ejection in the rat. Neuroendocrinology. 39:1984;563-572.
34. Stone T.W. Microiontophoresis and pressure injection. 1985;Wiley, New York.
35. Finn P.D., Yahr P. Projection of the sexually dimorphic area of the gerbil hypothalamus to the retrorubral field is essential for male sexual behavior. role of A8 and other cells Behav Neurosci. 108:1994;362-378.
36. Sayag N., Hoffman N.W., Yahr P. Telencephalic connections of the sexually dimorphic area of the gerbil hypothalamus that influence male sex behavior. Behav Neurosci. 8:1994;743-757.
37. Swanson L.W. Brain Maps. Structure of the Rat Brain:1992;Elsevier, Amsterdam.
38. Salter F.C. A morphological study of the lateral olfactory areas of the telencephalon in the Mongolian gerbil, Meriones unguiculatus. J Hirnforschung. 16:1975;223-244.
39. Yahr P., Newman A., Stephens D.L. Sexual behavior and scent marking in male gerbils. comparison of changes after castration and testosterone replacement Horm Behav. 13:1979;175-184.
40. DeVries G.J., Gonzales C.L., Yahr P. Afferent connections of the sexually dimorphic area of the hypothalamus of male and female gerbils. J Comp Neurol. 271:1988;91-105.
41. Finn P.D., DeVries G.J., Yahr P. Efferent projections of the sexually dimorphic area of the gerbil hypothalamus. anterograde identification and retrograde verification in males and females J Comp Neurol. 338:1993;491-520.
42. Coolen L.M., Wood R.I. Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain. simultaneous anterograde and retrograde tract tracing J Comp Neurol. 399:1998;189-209.
43. Giantonio G.W., Lund N.L., Gerall A.A. Effect of diencephalic and rhinencephalic lesions on the male rat's sexual behavior. J Comp Physiol Psychol. 73:1970;38-46.
44. Harris S.V., Sachs B.D. Copulatory behavior in male rats following amygdaloid lesions. Brain Res. 86:1975;514-518.
45. Kondo Y., Yamanouchi K. The possible involvement of the nonstrial pathway of the amygdala in neural control of sexual behavior in male rats. Brain Res Bull. 38:1995;37-40.
46. Davis B.J., Macrides F., Young W.M., Schneider S.P., Rosene D.L. Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster. Brain Res Bull. 3:1978;59-72.
47. Powers J.B., Winans S.S. Vomeronasal organ. critical role in mediating sexual behavior of the male hamster Science. 187:1975;961-963.
48. Scalia F., Winans S.S. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol. 161:1975;31-55.
49. Winans S.S., Powers J.B. Olfactory and vomeronasal deafferentation of male hamsters. histological and behavioral analyses Brain Res. 126:1977;325-344.
50. Wood R.I., Brabec R.K., Swann J.M., Newman S.W. Androgen and estrogen concentrating neurons in chemosensory pathways of the male Syrian hamster brain. Brain Res. 596:1992;89-98.
51. Wood R.I., Newman S.W. Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster brain. J Neurosci. 15:1995;7261-7269.
52. Wood R.I., Newman S.S. Hormonal influence on neurons of the mating behavior pathway in male hamsters. Micevych P.E., Hammer R.P. Jr. Neurobiological Effects of Sex Steroid Hormones. 1995;3-39 Cambridge University Press, Cambridge, UK.
53. Commins D., Yahr P. Autoradiographic localization of estrogen and androgen receptors in the sexually dimorphic area and other regions of the gerbil brain. J Comp Neurol. 231:1985;473-489.
54. Cheal M.L., Domesick V.B. Mating in male Mongolian gerbils after olfactory bulbectomy. Physiol Behav. 22:1979;199-202.
55. Barfield R.J., Sachs B.D. Sexual behavior. stimulation by painful electrical shock to skin in male rats Science. 161:1968;392-395.
56. Caggiula A.R., Eibergen R. Copulation of virgin male rats evoked by painful peripheral stimulation. J Comp Physiol Psychol. 69:1969;414-419.
57. Crowley W.R., Popolow H.B., Ward O.B. Jr. From dud to stud. copulatory behavior elicited through conditioned arousal in sexually inactive male rats Physiol Behav. 10:1973;391-394.
58. Smith W.J., Stewart J., Pfaus J.G. Tail pinch induces Fos immunoreactivity within several regions of the male rat brain. effects of age Physiol Behav. 61:1997;717-723.
59. Romero L.M., Levine S., Sapolsky R.M. Patterns of adrenocorticotropin secretagog release in response to social interactions and various degrees of novelty. Psychoneuroendocrinology. 20:1995;183-191.
60. Gomez D.M., Newman S.W. Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster. J Comp Neurol. 317:1992;195-218.
61. Neurons of origin and fiber trajectory of amygdalofugal projections to the medial preoptic area in Syrian hamsters. J Comp Neurol. 280:1989;59-71.
62. Morin L.P., Goodless-Sanchez N., Smale L., Moore R.Y. Projections of the suprachiasmatic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster. Neuroscience. 61:1994;391-410.
63. Simerly R.B., Swanson L.W. The organization of neural inputs to the medial preoptic nucleus of the rat. J Comp Neurol. 246:1986;312-342.
64. Simerly R.B., Swanson L.W. Projections of the medial preoptic nucleus. a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat J Comp Neurol. 270:1988;209-242.
65. Kondo Y., Arai Y. Functional association between the medial amygdala and the medial preoptic area in regulation of mating in the male rat. Physiol Behav. 57:1995;69-73.
66. Bottjer S.W., Miesner E.A., Arnold A.P. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science. 224:1984;901-903.
67. Ledoux J.E., Ruggiero D.A., Forest R., Stornetta R., Reis D.J. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol. 264:1987;123-146.
68. Namura S., Takada M., Kikuchi H., Mizuno N. Collateral projections of single neurons in the posterior thalamic region to both the temporal cortex and the amygdala. a fluorescent retrograde double-labeling study in the rat J Comp Neurol. 384:1997;59-70.
69. Gabriel M., Saltwick S.E., Miller J.D. Conditioning and reversal of short-latency multiple-unit responses in the rabbit medial geniculate nucleus. Science. 189:1975;1108-1109.
70. Ryugo D.K., Weinberger N.M. Differential plasticity of morphologically distinct neuron populations in the medial geniculate body of the cat during classical conditioning. Behav Biol. 22:1978;275-301.
71. Amir S., Stewart J. Induction of Fos expression in the circadian system by unsignaled light is attenuated as a result of previous experience with signaled light. a role for Pavlovian conditioning Neuroscience. 83:1998;657-661.
72. Brown R.E., Murdoch T., Murphy P.R., Moger W.H. Hormonal responses of male gerbils to stimuli from their mates and pups. Horm Behav. 29:1995;474-491.
73. Elwood R.W. Changes in the responses of male and female gerbils (Meriones unguiculatus) towards test pups during the pregnancy of the female. Anim Behav. 25:1977;46-51.
74. Elwood RW, Ostermeyer MC Infanticide by male and female Mongolian gerbils: ontogeny, causation, and function. In: Hausfater G, Hrdy SB, editors. Infanticide: Comparative and Evolutionary Perspectives. New York: Aldine; 1984. pp. 367-86.
75. Jakubowski M., Terkel J. Transition from pup killing to parental behavior in male and virgin female albino rats. Physiol Behav. 34:1985;683-686.
76. Mennella J.A., Moltz H. Infanticide in rats. male strategy and female counter-strategy Physiol Behav. 42:1988;19-28.
77. vom Saal F.S. Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice. Physiol Behav. 34:1985;7-15.
78. Numan M. Maternal behavior. Knobil E., Neill J.D. The Physiology of Reproduction, vol 2. 2nd ed:1994;221-302 Raven Press, New York.
79. Kirkpatrick B., Kim J.W., Insel T.R. Limbic system Fos expression associated with parental behavior. Brain Res. 658:1994;112-118.
80. Simerly R.B., Gorski R.A., Swanson L.W. The neurotransmitter specificity of cells and fibers in the medial preoptic nucleus. an immunohistochemical study in the rat J Comp Neurol. 246:1986;364-381.