Laterally asymmetrical cell number in a sexually dimorphic nucleus in the gerbil hypothalamus is correlated with vocal emission rates

Behavioral Neuroscience

Volumn 112, Issue 4, 1998, Pages 979-990

  Holman, Steve D ^a   Janus, Christopher ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

TESTOSTERONE;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; BRAIN ASYMMETRY; CELL COUNT; CELL STRUCTURE; CELL VOLUME; FEMALE; GERBIL; HYPOTHALAMUS; MALE; NONHUMAN; SEX DIFFERENCE; STEREOLOGY; VERBAL COMMUNICATION;

EID: 0031688142     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.112.4.979     Document Type: Article

References (84)

1. Arai, Y., Murakami, S., & Nishizuka, M. (1994). Androgen enhances neuronal degeneration in the developing preoptic area: Apoptosis in the anteroventral periventricular nucleus (AVPvN-POA). Hormones and Behavior, 28, 313-319.
2. Arai, Y., Sekine, Y., & Murakami, S. (1996). Estrogen and apoptosis in the developing sexually dimorphic preoptic area in female rats. Neuroscience Research, 25, 403-407.
3. Arnold, A. P., & Bottjer, S. W. (1985), Cerebral lateralisation in birds. In S. D. Glick (Ed.), Cerebral lateralisation in nonhuman species (pp. 11-40). London: Academic Press.
4. Arnold, A. P., & Breedlove, S. M. (1985). Organizational and activational effects of sex steroids on brain and behavior: A reanalysis. Hormones and Behavior, 19, 469-498.
5. Baddeley, A. J., Gundersen, H. J. G., & Cruz-Orive, L. M. (1986). Estimation of surface area from vertical sections. Journal of Microscopy, 142, 259-276.
6. Braendgaard, H., Evans, S. M., Howard, C. V., & Gundersen, H. J. G. (1990). Total number of neurons in human neocortex unbiasedly estimated using optical disector. Journal of Microscopy, 157, 285-304.
7. Brown, N. A., McCarthy, A., & Wolpert, L. (1991). Development of handed body asymmetry in mammals. CIBA Foundation Symposia, 162, 182-201.
8. Burton, G. J., & Palmer, M. E. (1988). Eradicating fetomaternal fluid shift during perfusion fixation of the human placenta. Placenta, 9, 327-332.
9. Coggeshall, R. E., & Lekan, H. A. (1996). Methods for determining numbers of cells and synapses: A case for more uniform standards of review. Journal of Comparative Neurology, 364, 6-15.
10. Collado, P., Beyer, C., Hutchison, J. B., & Holman, S. D. (1995). Hypothalamic distribution of astrocytes is gender-related in Mongolian gerbils. Neuroscience Letters, 184, 86-89.
11. Cruz-Orive, L. M., & Myking, A. O. (1981). Stereological estimation of volume ratios by systematic sections. Journal of Microscopy, 122, 143-157.
12. Cruz-Orive, L. M., & Weibel, E. R. (1990). Recent Stereological methods for cell biology: A brief survey. American Journal of Physiology, 258, L148-L156.
13. Davidson, R. J., & Hugdahl, K. (1995). Brain asymmetry. Cambridge, MA: MIT Press.
14. Davis, E. C., Popper, P., & Gorski, R. A. (1996). The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Research, 734, 10-18.
15. Diamond, M. C. (1983). New data supporting cortical asymmetry in males and females. Behavioral Brain Science, 3, 233-224.
16. Finlay, B. L., & Slattery, M. (1983). Local differences in the amount of early cell death in neocortex predict adult local specializations. Science, 219, 1349-1351.
17. Floody, O. W., & Arnold, A. P. (1997). Song lateralization in the zebra finch. Hormones and Behavior, 31, 25-34.
18. Galaburda, A. M. (1995). Anatomic basis of cerebral dominance. In J. R. Davidson & K. Hugdahl (Eds.), Brain asymmetry (pp. 51-73). Cambridge, MA: MIT Press.
19. Galaburda, A. M., Aboitiz, F., Rosen, G. D., & Sherman, G. F. (1986). Histological asymmetry in the primary visual cortex of the rat: Implications for mechanisms of cerebral asymmetry. Cortex, 22, 151-160.
20. Galaburda, A. M., Rosen, G. D., & Sherman, G. F. (1990), Individual variability in cortical organization: Its relationship to brain laterally and implications to function. Neuropsychologia, 28, 529-546.
21. Galaburda, A. M., Sanides, F., & Geschwind, N. (1978). Human brain: Cytoarchitectonic left-right asymmetries in the temporal speech region. Archives in Neurology, 35, 812-827.
22. Cannon, P. J., Holloway, R. L., Broadfield, D. C., & Braun, A. R. (1998). Asymmetry of chimpanzee planum temporale: Human-like pattern of Wernicke's brain area homolog. Science, 279, 220-222.
23. Geschwind, A. M., & Levitsky, W. (1978). Human brain: Left-right asymmetries in temporal speech region. Science, 161, 186-187.
24. Geschwind, N., & Behan, P. (1984). Laterality, hormones, and immunity. In N. Geshwind & A. M. Galaburda (Eds.), Cerebral dominance: The biological foundations (pp. 211-214). Cambridge, MA: Harvard University Press.
25. Geschwind, N., & Galaburda, A. M. (1985). Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Archives of Neurology, 42, 428-458.
26. Goller, F., & Suthers, R. A. (1995). Implications for lateralization of bird song from unilateral gating of bilateral motor patterns. Nature, 373, 63-66.
27. Coller, F., & Suthers, R. A. (1996a). Role of syringeal muscles in controlling the phonology of bird song. Journal of Neurophysiology, 76, 287-300.
28. Goller, F., & Suthers, R. A. (1996b). Role of syringeal muscles in gating air-flow and sound production in singing brown thrashers. Journal of Neurophysiology, 75, 867-876.
29. Gundersen, H. J. G. (1977). Notes on the estimation of the numerical density of arbitrary profiles: The edge effect. Journal of Microscopy, 111, 219-223.
30. Gundersen, H. J. G. (1988). The nucleator. Journal of Microscopy, 151, 3-21.
31. Gundersen, H. J. G., Bagger, P., Bendsten, T. P., Evans, S. M., Korbo, L., Marcussen, N., Møller, A., Nielsen, K., Nyengaard, J. R., Battenberg, P., Sørensen, F. B., Vesterby, A., & West, M. J. (1988). The new stereological tools: Disector, fractionator, nucleator and points sample intercepts and their use in pathological research and diagnosis. Acta Pathologica Microbiologica Immulogica Scandinavica, 96, 857-881.
32. Gundersen, H. J. G., Bendsten, T. F., Korbo, L., Marcussen, N., Møller, A., Nielsen, K., Nyengaard, J. R., Pakkenberg, B., Sørensen, F. B., Vesterby, A., & West, M. J. (1988). Some new simple and efficient stereological methods and their use in pathological research and diagnosis. Acta Pathohgica Microbiologica Immulogica Scandinavica, 96, 379-394.
33. Gundersen, H. J. G., & Jensen, E. B. (1987). The efficiency of systematic sampling in stereology and its prediction. Journal of Microscopy, 147, 229-262.
34. Gundersen, H. J. G., & Østerby, R. (1981). Optimizing sampling efficiency of stereological studies in biology: "Do more less well!" Journal of Microscopy, 121, 65-73.
35. Hart, B. L., & Leedy, M. G. (1985). Neurological bases of male sexual behavior. In N. Adler, D. W. Pfaff, & R. W. Goy (Eds.), Reproduction: Handbook of behavioral neurobiology (pp. 373-422). New York: Plenum.
36. Heilman, K. M. (1995). Attentional asymmetries. In J. R. Davidson & K. Hugdahl (Eds.), Brain asymmetry (pp. 51-73). Cambridge, MA: MIT Press.
37. Holman, S. D. (1981). Neonatal androgenic influences on masculine ultrasonic vocalizations of Mongolian gerbils. Physiology and Behavior, 26, 583-586.
38. Holman, S. D. (in press). Neuronal cell death during sexual differentiation and lateralization of vocal communication. Neuroscience & Biobehavior Review.
39. Holman, S. D., & Collado, P. (1998). Lateralized cell proliferation and apoptosis in a sexually differentiating hypothalamic nucleus. Manuscript in preparation.
40. Holman, S. D., Collado, P., Rice, A., & Hutchison, J. B. (1995). Stereological estimates of postnatal structural differentiation in a sexually dimorphic hypothalamic nucleus involved in vocal control. Brain Research, 694, 167-176.
41. Holman, S. D., Collado, P., Skepper, J. N., & Rice, A. (1996). Postnatal development of a sexually dimorphic, hypothalamic nucleus in gerbils: A stereological study of neuronal number and apoptosis. Journal of Comparative Neurology, 376, 315-325.
42. Holman, S. D., & Hutchison, J. B. (1982). Pre-copulatory behaviour in the male Mongolian gerbil: I. Differences in dependence on androgen of component patterns. Animal Behaviour, 30, 221-230.
43. Holman, S. D., & Hutchison, J. B. (1991a). Differential effects of neonatal castration on the development of sexually dimorphic brain areas. Developmental Brain Research, 61, 147-150.
44. Holman, S. D., & Hutchison, J. B. (1991b). Lateralized action of androgen on development of behavior and brain sex differences. Brain Research Bulletin, 27, 261-265.
45. Holman, S. D., & Hutchison, J. B. (1993). Lateralization of a sexually dimorphic brain area associated with steroid-sensitive behavior in the male gerbil. Behavioral Neuroscience, 107, 186-193.
46. Holman, S. D., & Hutchison, J. B. (1994). Is courtship vocal communication related to asymmetric mechanisms in the brain? In F. Farrabolini (Ed.), Aggression, gender and sex: Psychobiological and psychosexual studies in animals and humans (Vol. 3, pp. 223-234). London: Wiley-Liss.
47. Holman, S. D., & Rice, A. (1996). Androgenic effects on hypothalamic asymmetry in a sexually differentiated nucleus related to vocal behavior in Mongolian gerbils. Hormones and Behavior, 30, 662-672.
48. Kawata, M (1995). Role of steroid hormones and their receptors in structural organization in the nervous system. Neuroscience Research, 42, 1-46.
49. Lewis, D. W., & Diamond, M. C. (1995). The influence of gonadal steroids on the asymmetry of the cerebral cortex. In J. R. Davidson & K. Hugdahl (Eds.), Brain asymmetry (pp. 51-73). Cambridge, MA: MIT Press.
50. Lowe, L. A., Supp, D. M., Sampath, K., Yokoyama, T., Wright, C. V. E., Potter, S. S., Overbeek, P., & Kuehn, M. R. (1996). Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature, 381, 158-161.
51. Mayhew, T. M. (1991). The new stereological methods for interpreting functional morphology from slices of cells and organs. Experimental Physiology, 76, 639-665.
52. Meno, C., Saijoh, Y., Fujii, H., Ikeda, M., Yokoyama, T., Yokoyama, M., Toyoda, Y., & Hamada, H. (1996). Left-right asymmetric expression of the TGFβ-family member lefty in mouse embryos. Nature, 381, 151-155.
53. Michael, R. P., & Cruz-Orive, L. M. (1988). Application of the Cavalieri principle and vertical sections method to lung: Estimation of volume and pleural surface area. Journal of Microscopy, 150, 117-136.
54. Møller, A., Strange, P., & Gundersen, H. J. G. (1990). Efficient estimation of cell volume and number using the nucleator and disector. Journal of Microscopy, 159, 61-71.
55. Naruse, I., & Keino, H. (1995). Apoptosis in the developing CNS. Progress in Neurobiology, 47, 135-155.
56. Nordeen, E. J., Nordeen, K. W., Sengelaub, D. R., & Arnold, A. P. (1985). Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science, 229, 671-673.
57. Nordeen, E. J., & Yahr, P. (1982). Hemispheric asymmetries in the behavioral and hormonal effects of sexually differentiating mammalian brain. Science, 218, 391-394.
58. Nottebohm, F. (1977). Asymmetries in neural control of vocalizations in the canary. In S. Harnad, R. W. Doty, L. Goldstein, J. Jaynes, & G. Krauthamer (Eds.), Lateralization in the nervous system (pp. 23-44). New York: Academic Press.
59. Nottebohm, F., & Nottebohm, M. (1976). Left hypoglossal dominance in the control of canary and white-crowned sparrow song. Journal of Comparative Physiology, 108, 171-192.
60. Pakkenberg, B., & Gundersen, H. J. G. (1988). Total number of neurons and glial cells in human brain nuclei estimated by the disector and the fractionator. Journal of Microscopy, 150, 1-20.
61. Paton, J. A., & Manogue, K. R. (1982). Bilateral interactions within vocal control pathway of birds: Two evolutionary alternatives. Journal of Comparative Neurology, 212, 239-335.
62. Peters, A., Palay, S. L., & Webster, H. D. (1991). The fine structure of the nervous system: Neurons and their supporting cells. Oxford, England: OUP.
63. Probst, B. (1987). Developmental changes in the pituitary-gonadal-axis in male Mongolian gerbils from birth to adulthood. Experimental Clinical Endocrinology, 90, 157-166.
64. Roberts, L. H. (1975a). The functional anatomy of the rodent larynx in relation to audible and ultrasonic cry production. Zoological Journal of the Linnean Society, 56, 255-264.
65. Roberts, L. H. (1975b). The rodent ultrasound producation mechanism. Ultrasonics, 13, 83-88.
66. Robinson, T. E., Becker, J. B., & Camp, D. M. (1984). Sex differences in behavioral and brain asymmetries. In M. Myslobodsky (Ed.), Hemisyndromes: Psychobiology, neurology, psychiatry (pp. 91-128). New York: Academic Press.
67. Robinson, T. E., Becker, J. B., Camp, D. M., & Mansour, A. (1985). Variations in the pattern of behavioral and brain asymmetries due to sex differences. In S. D. Glick (Ed.), Cerebral lateralization in nonhuman species (pp. 185-233). Orlando, FL: Academic Press.
68. Rosen, G. D. (1996). Cellular, morphometric, ontogenetic and connectional substrates of anatomical asymmetry. Neuroscience and Biobehavioral Reviews, 20, 607-615.
69. Rosen, G. D., Sherman, G. F., & Galaburda, A. M. (1989). Interhemispheric connections differ between symmetrical and asymmetrical brain regions. Neuroscience, 33, 525-533.
70. Rosen, G. D., Sherman, G. F., & Galaburda, A. M. (1991). Ontogenesis of neocortical asymmetry: A [3H]thymidine study. Neuroscience, 41, 779-790.
71. Sengelaub, D., Jacobs, L. F., & Finlay, B. L. (1985). Regional differences in normally occurring cell death in the developing hamster lateral geniculate nuclei. Neuroscience Letters, 55, 103-108.
72. Shaywitz, B. A., Shaywitz, S. E., Pugh, K. R., Constable, R. T., Skudlarski, P., Fulbright, R. K., Bronen, R. A., Fletcher, J. M., Shankweller, D. P., Katz, L., & Gore, J. C. (1995). Sex differences in the functional organization of the brain for language. Nature, 373, 607-609.
73. Sherman, G. F., Galaburda, A. M., & Geschwind, N. (1992). Neuroanatomical asymmetries in non-human species. Trends in Neurosciences, 5, 429-431.
74. Suthers, R. A. (1990). Contributions to birdsong from the left and right sides of the intact syrinx. Nature, 347, 473-477.
75. Suthers, R. A. (1994). Variable asymmetry and resonance in the avian vocal-tract - A structural basis for individually distinct vocalizations. Journal of Comparative Physiology A - Sensory Neural and Behavioral Physiology, 175, 457-466.
76. Ulibarri, C., & Yahr, P. (1993). Ontogeny of the sexually dimorphic area of the gerbil hypothalamus. Developmental Brain Research, 74, 14-24.
77. Ulibarri, C., & Yahr, P. (1996). Effects of androgens and estrogens on sexual differentiation of sex behavior, scent marking and the sexually dimorphic area of the gerbil hypothalamus. Hormones & Behavior, 30, 107-130.
78. Weibel, E. R. (1979). Stereological methods. Volume 1: Practical methods for biological morphometry, London: Academic Press.
79. Wetzel, D. M., Kelley, D. B., & Campbell, B. A. (1980). Central control of ultrasonic vocalizations in neonatal rats: I. Brain stem nuclei. Journal of Comparative Physiology and Psychology, 94, 596-605.
80. Witelson, S. F. (1976). Sex and the single hemisphere: Right hemisphere specialization for spatial processing. Science, 193, 425-427.
81. Witelson, S. F. (1991). Neural sexual mosaicism: Sexual differentiation of the human temporo-parietal region for functional asymmetry. Psychoneuroendocrinology, 16, 131-151.
82. Yahr, P., Finn, P. D., Hoffman, N. W., & Sayag, N. (1994). Sexually dimorphic cell groups in the medial preoptic area that are essential for male sex behavior and the neural pathways needed for their effects. Psychoneuroendocrinology, 19, 463-470.
83. Yahr, P., & Gregory, J. E. (1993). 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 Research, 631, 287-296.
84. Yahr, P., & Jacobsen. (1994). Hypothalamic knife cuts that disrupt mating in male gerbils sever efferents and forebrain afferents of the sexually dimorphic area. Behavioral Neuroscience, 108, 735-742.