Hypothalamic Growth-Related Cellular Phenomena and Brain Stem-Cord Motor Control Phenomena in a Weil-Defined Vertebrate Neuroendocrine Circuit

  • D. W. Pfaff
  • A. Robbins
Conference paper

Abstract

Determining the factors which modulate activity of specific cell groups in the brain requires detailed enough understanding of the particular circuits involved that experimental measurements can be set up with precision and critical interpretations can be applied in a sophisticated manner. The neural circuit for a primary female reproductive behavior, lordosis behavior, has been determined (Pfaff 1980; Pfaff and Schwartz-Giblin 1988). Certain strategic advantages allowed this to be the first one completed for a vertebrate behavior, namely relatively simple stimuli and responses, and an exquisite dependence on steroid hormone action in the hypothalamus. The power of estrogenic and progestin actions in facilitating lordosis behavior permitted us to use these steroid hormones as chemically defined triggers for the close analysis of neural mechanisms, and allowed us to relate neurobiological to molecular biological approaches. Using steroid hormone autoradiography, precise locations of neurons with steroid sex hormone receptors were mapped (Pfaff 1968; Pfaff and Keiner 1973; Pfaff 1975; Morrell and Pfaff 1978). An important aspect was the generality of several features of these hormone-binding neurons across all vertebrate species examined (Pfaff 1976; Morrell and Pfaff 1978; McEwen et al. 1979). Not only were the existence and locations of estrogen, androgen, and progestin binding neurons often reliable from species to species, but they also could be correlated well with neural events controlling reproductive physiology.

Keywords

Estrogen Testosterone Neurol Progesterone Alanine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adler NT, Davis PG, Komisaruk BR (1977) Variation in the size and sensitivity of a genital sensory field in relation to the estrous cycle in rats. Horm Behav 9: 334–344PubMedCrossRefGoogle Scholar
  2. Atmar VJ, Kuehn GD (1981) Phosphorylation of ornithine decarboxylase by a polyamine-dependent protein kinase. Proc Natl Acad Sci USA 78: 5518–5522PubMedCrossRefGoogle Scholar
  3. Baserga R (1981) Introduction to cell growth: growth in size and DNA replication; In: Baserga R (ed) Tissue growth factors. Springer, Berlin Heidelberg New York, pp 1–12Google Scholar
  4. Baserga R (1985) The biology of cell reproduction. Harvard University Press, Cambridge, MAGoogle Scholar
  5. Baserga R, Estensen RD, Petersen RO (1965) Inhibition of DNA synthesis in Ehrlich ascites cells by actinomycin D. II: the presynaptic block in the cell cycle. Proc Natl Acad Sci USA 54: 1141–1148PubMedCrossRefGoogle Scholar
  6. Bermant G, Westbrook W (1966) Peripheral factors in the regulation of sexual contact by female rats. J Comp Physiol Psychol 61: 244–250PubMedCrossRefGoogle Scholar
  7. Brink EE, Pfaff DW (1980) Vertebral muscles of the back and tail of the albino rat (Rattus norvegicus albinus). Brain Behav Evol 17: 1–47PubMedCrossRefGoogle Scholar
  8. Brink EE, Pfaff DW (1981) Supraspinal and segmental input to lumbar epaxial motoneurons in the rat. Brain Res 226: 43–60PubMedCrossRefGoogle Scholar
  9. Brink EE, Morrell JI, Pfaff DW (1979) Localization of lumbar epaxial motoneurons in the rat. Brain Res 170: 23–41PubMedCrossRefGoogle Scholar
  10. Brink EE, Modianos DT, Pfaff DW (1980) Ablations of lumbar epaxial musculature: effects on lordosis behavior of female rats. Brain Behav Evol 17: 67–88PubMedCrossRefGoogle Scholar
  11. Carrer HF, Aoki A (1982) Ultrastructural changes in the hypothalamic ventromedial nucleus of ovariectomized rats after estrogen treatment. Brain Res 240: 221–223PubMedCrossRefGoogle Scholar
  12. Chung SK, Cohen RS, Pfaff DW (1984) Ultrastructure and enzyme digestion of nucleoli and associated structures in hypothalamic nerve cells viewed in resinless sections. Biol Cell 51: 23–34PubMedGoogle Scholar
  13. Chung SK, Pfaff DW, Cohen RS (1988) Estrogen-induced alterations in synaptic morphology in the midbrain central gray. Exp Brain Res 69: 522–530PubMedCrossRefGoogle Scholar
  14. Chung SK, Pfaff DW, Cohen RS (1989a) Projections of ventromedial hypothalamic neurons to the midbrain central gray: an ultrastructural study. Neuroscience (in press)Google Scholar
  15. Chung SK, Pfaff DW, Cohen RS (1989b) Transsynaptic degeneration in midbrain central gray after VMN lesions: a qualitative and quantitative analysis. Neuroscience (in press)Google Scholar
  16. Cohen MS, Schwartz-Giblin S, Pfaff DW (1985) The pudendal nerve-evoked response in axial muscle. Exp Brain Res 61: 175–185PubMedCrossRefGoogle Scholar
  17. Cohen MS, Schwartz-Giblin S, Pfaff DW (1987a) Effects of total and partial spinal transections on the pudendal nerve-evoked response in rat lumbar axial muscle. Brain Res 401: 103–112PubMedCrossRefGoogle Scholar
  18. Cohen MS, Schwartz-Giblin S, Pfaff DW (1987b) Brainstem reticular stimulation facilitates back muscle motoneuronal responses to pudendal nerve input. Brain Res 405: 155–158PubMedCrossRefGoogle Scholar
  19. Cohen R, Pfaff DW (1981) Ultrastructure of neurons in the ventromedial nucleus of the hypothalamus in ovariectomized rats with or without estrogen treatment. Cell Tissue Res 217: 451–470PubMedCrossRefGoogle Scholar
  20. Cohen RS, Chung SK, Pfaff DW (1984) Alteration by estrogen of the nucleoli in nerve cells of the rat hypothalamus. Cell Tissue Res 235: 485–489PubMedCrossRefGoogle Scholar
  21. Cottingham SL, Pfaff DW (1987) Electrical stimulation of the midbrain central gray facilitates lateral vestibulospinal activation of back muscle EMG in the rat. Brain Res 421: 397–400PubMedCrossRefGoogle Scholar
  22. Cottingham SL, Femano PA, Pfaff DW (1987) Electrical stimulation of the midbrain central gray facilitates reticulospinal activation of axial muscle EMG. Exp Neurol 97: 704–724PubMedCrossRefGoogle Scholar
  23. Cottingham SL, Femano PA, Pfaff DW (1988) Vestibulospinal and reticulospinal interactions in the activation of back muscle EMG in the rat. Exp Brain Res 73: 198–208PubMedCrossRefGoogle Scholar
  24. Dethlefsen LA (1980) In quest of the quaint quiescent cells. In: Meyn RE, Withers HR (eds) Radiation biology in cancer research. Raven, New York, pp 415–435Google Scholar
  25. Diakow C, Pfaff DW, Komisaruk B (1973) Sensory and hormonal interactions in eliciting lordosis. Fed Proc 32: 241Google Scholar
  26. Femano PA, Schwartz-Giblin S, Pfaff DW (1984a) Brainstem reticular influences on lumbar axial muscle activity. I. Effective sites. Am J Physiol 246: R389–R395PubMedGoogle Scholar
  27. Femano PA, Schwartz-Giblin S, Pfaff DW (1984b) Brainstem reticular influences on lumbar axial muscle activity. II. Temporal aspects. Am J Physiol 246: R396–R401PubMedGoogle Scholar
  28. Fox JE (1970) Reticulospinal neurones in the rat. Brain Res 23: 35–40PubMedCrossRefGoogle Scholar
  29. Galanti N, Jonak GJ, Soprano KJ, Floros J, Kaczmarek L, Weissman S, Reddy VB, Tilghman SM, Baserga R (1981) Characterization and biological activity of cloned simian virus 40 DNA fragments. J Biol Chem 256: 6469–6474PubMedGoogle Scholar
  30. Gelfant S (1977) A new concept of tissue and tumor cell proliferation. Cancer Res 37: 3845–3862PubMedGoogle Scholar
  31. Hart BL (1969) Gonadal hormones and sexual reflexes in the female rat. Horm Behav 1: 65–71CrossRefGoogle Scholar
  32. Heby O, Janne J (1981) Polyamine antimetabolites: biochemistry, specificity and biological effects of inhibitors of polyamine synthesis. In: Morris DR, Marton LJ (eds) Polyamines in biology and medicine. Marcel Dekker, New York, pp 243–310Google Scholar
  33. Hornby JB, Rose JD (1976) Responses of caudal brain stem neurons to vaginal and somatosensory stimulation in the rat and evidence of genital-nociceptive interactions. Exp Neurol 51: 363–376PubMedCrossRefGoogle Scholar
  34. Jaehning JA, Stewart CC, Roeder RG (1975) DNA dependent RNA polymerase levels during the response of human peripheral lymphocytes to phytohemagglutinin. Cell 4: 51–57PubMedCrossRefGoogle Scholar
  35. Jones KJ, Pfaff DW (1989) Emerging tenets of steroid hormone action on the brain. In: Motta M (ed) Comprehensive endocrinology. Raven, New YorkGoogle Scholar
  36. Jones KJ, Pfaff DW, McEwen BS (1985) Early estrogen-induced nuclear changes in rat hypothalamic ventromedial neurons: an ultrastructural and morphometric analysis. J Comp Neurol 239: 255–266PubMedCrossRefGoogle Scholar
  37. Jones KJ, Chikaraishi DM, Harrington CA, McEwen BS, Pfaff DW (1986) In situ hybridization detection of estradiol-induced changes in ribosomal RNA levels in rat brain. Mol Brain Res 1: 145–152CrossRefGoogle Scholar
  38. Jones KJ, McEwen BS, Pfaff DW (1987) Quantitative assessment of the synergistic and independent effects of estradiol and progesterone on ventromedial hypothalamic and preoptic-area proteins in female rat brain. Metab Brain Dis 2: 271–281PubMedCrossRefGoogle Scholar
  39. Jones KJ, McEwen BS, Pfaff DW (1988) Quantitative assessment of early and discontinuous estradiol-induced effects on ventromedial hypothalamic and preoptic area proteins in female rat brain. Neuroendocrinology 48: 561–568PubMedCrossRefGoogle Scholar
  40. Jones KJ, Chikaraishi D, Harrington C, Pfaff D (1989) Estrogen induction of ribosomal RNA precursor shown by in situ hybridization. Neuron (in press)Google Scholar
  41. Kawata M, McCabe JT, Harrington C, Chikaraishi D, Pfaff DW (1988) In situ hybridization analysis of osmotic stimulus-induced changes in ribosomal RNA in rat supraoptic nucleus. J Comp Neurol 270: 528–536PubMedCrossRefGoogle Scholar
  42. Komisaruk BR, Diakow C (1973) Lordosis reflex intensity in rats in relation to the estrous cycle, ovariectomy, estrogen and administration and mating behavior. Endocrinology 93: 548–557PubMedCrossRefGoogle Scholar
  43. Komisaruk BR, Adler NT, Hutchison J (1972) Genital sensory field: enlargement by estrogen treatment in female rats. Science 178: 1295–1298PubMedCrossRefGoogle Scholar
  44. Kow LM, Pfaff DW (1973/74) Effect of estrogen treatment on the size of the receptive field and response threshold of pudendal nerve in the female rat. Neuroendocrinology 13:299–313CrossRefGoogle Scholar
  45. Kow LM, Pfaff DW (1975) Dorsal root recording relevant for mating reflexes in female rats: identification of receptive fields and effects of peripheral denervation. J Neurobiol 6: 23–37PubMedCrossRefGoogle Scholar
  46. Kow LM, Pfaff DW (1976) Sensory requirements for the lordosis reflex in female rats. Brain Res 101: 47–66PubMedCrossRefGoogle Scholar
  47. Kow LM, Pfaff DW (1979) Responses of single units in sixth lumbar dorsal root ganglion of female rats to mechanostimulation relevant for lordosis reflex. J Neurophysiol 42: 203–213PubMedGoogle Scholar
  48. Kow LM, Pfaff DW (1982) Responses of medullary reticulospinal and other reticular neurons to somatosensory and brainstem stimulation in anesthetized or freely-moving ovariectomized rats with or without estrogen treatment. Exp Brain Res 47: 191–202PubMedCrossRefGoogle Scholar
  49. Kow LM, Montgomery MO, Pfaff DW (1977) Effects of spinal cord transections on lordosis reflex in female rats. Brain Res 123: 75–88PubMedCrossRefGoogle Scholar
  50. Kow LM, Montgomery MO, Pfaff DW (1979) Triggering of lordosis reflex in female rats with somatosensory stimulation: quantitative determination of stimulus parameters. J Neurophysiol 42: 195–202PubMedGoogle Scholar
  51. Kow LM, Zemlan FP, Pfaff DW (1980) Responses of lumbosacral spinal units to mechanical stimuli related to analysis of lordosis reflex in female rats. J Neurophysiol 43: 27–45PubMedGoogle Scholar
  52. Lieberman I, Abrams R, Ove P (1963) Changes in the metabolism of ribonucleic acid preceding the synthesis of deoxyribonucleic acid in mammalian cells cultured from the animal. J Biol Chem 238: 2141–2149PubMedGoogle Scholar
  53. Martin GF, Vertes RP, Waltzer R (1985) Spinal projections of the gigantocellular reticular formation in the rat. Evidence for projections from different areas to lamine I and II and lamina IX. Exp Brain Res 58: 154–162PubMedCrossRefGoogle Scholar
  54. Matsumoto A, Arai Y (1981) Neuronal plasticity in the deafferented hypothalamic arcuate nucleus of adult female rats and its enhancement by treatment with estrogen. J Comp Neurol 197: 197PubMedCrossRefGoogle Scholar
  55. McEwen BS, Davis PG, Parsons B, Pfaff DW (1979) The brain as a target for steroid hormone action. Annu Rev Neurosci 2: 65–112PubMedCrossRefGoogle Scholar
  56. McKenna KE, Nadelhaft I (1986) The organization of the pudendal nerve in the male and female rat. J Comp Neurol 248: 532–549PubMedCrossRefGoogle Scholar
  57. Meisel R, Pfaff DW (1985) Brain region specificity in estradiol effects on neuronal ultrastructure in rats. Mol Cell Endocrinol 40: 159–166PubMedCrossRefGoogle Scholar
  58. Mobbs CV, Harlan RE, Burrous MR, Pfaff DW (1988) An estradiol-induced protein synthesized in the ventral medial hypothalamus and transported to the midbrain central gray. J Neurosci 8: 113–118PubMedGoogle Scholar
  59. Mobbs C, Fink G, Johnson M, Welch W, Pfaff DW (1989) Co-migration on 2-D gels of an estrogen-induced brain protein, an LHRH-induced pituitary protein, and an uncoating ATPase/heat-shock 70Kd protein. Mol Cell Endocrinol (in press)Google Scholar
  60. Modianos DT, Pfaff DW (1977) Facilitation of the lordosis reflex in female rats by electrical stimulation of the lateral vestibular nucleus. Brain Res 134: 333–345PubMedCrossRefGoogle Scholar
  61. Modianos D, Pfaff DW (1979) Medullary reticular formation lesions and lordosis reflex in female rats. Brain Res 171: 334–338PubMedCrossRefGoogle Scholar
  62. Morrell JI, Pfaff DW (1978) A neuroendocrine approach to brain function: localization of sex steroid concentrating cells in vertebrate brains. Am Zool 18: 447–460Google Scholar
  63. Mueller C, Graessmann A, Graessmann M (1978) Mapping of early SV40-specific functions by microinjection of different early viral DNA fragments. Cell 15: 579–585PubMedCrossRefGoogle Scholar
  64. Pfaff DW (1968) Autoradiographic localization of radioactivity in rat brain after injection of tritiated sex hormones. Science 161: 1355–1356PubMedCrossRefGoogle Scholar
  65. Pfaff DW (1975) Theoretical consideration of cross-fiber pattern coding in the neural signalling of pheromones and other chemical stimuli. Psychoneuroendocrinology 1: 79–93CrossRefGoogle Scholar
  66. Pfaff DW (1976) The neuroanatomy of sex hormone receptors in the vertebrate brain. In: Kumar TCA (ed) Neuroendocrine regulation of fertility. Karger, Basel, pp 30–45Google Scholar
  67. Pfaff DW (1980) Estrogens and brain function: neural analysis of a hormone-controlled mammalian reproductive behavior. Springer, Berlin Heidelberg New YorkGoogle Scholar
  68. Pfaff DW, Keiner M (1973) Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol 151: 121–158PubMedCrossRefGoogle Scholar
  69. Pfaff DW, Lewis C (1974) Film analyses of lordosis in female rats. Horm Behav 5: 317–335PubMedCrossRefGoogle Scholar
  70. Pfaff DW, Schwartz-Giblin S (1988) Cellular mechanisms of female reproductive behaviors. In: Knobil E, Neill J, et al (eds) The physiology of reproduction. Raven, New York, pp 1487–1568Google Scholar
  71. Pfaff DW, Montgomery M, Lewis C (1977) Somatosensory determinants of lordosis in female rats: behavioral definition of the estrogen effect. J Comp Physiol Psychol 91: 134–145PubMedCrossRefGoogle Scholar
  72. Pfaff DW, Diakow C, Montgomery M, Jenkins FA (1978) X-ray cinematographic analysis of lordosis in female rats. J Comp Physiol Psychol 92 (5): 937–941CrossRefGoogle Scholar
  73. Riskind P, Moss RL (1979) Midbrain central gray: LHRH infusion enhances lordotic behavior in estrogen-primed ovariectomized rats. Brain Res Bull 4: 203–205PubMedCrossRefGoogle Scholar
  74. Riskind P, Moss RL (1983) Effects of lesions of putative LHRH-containing pathways and midbrain nuclei on lordotic behavior and luteinizing hormone release in ovariectomized rats. Brain Res Bull 11: 493–500PubMedCrossRefGoogle Scholar
  75. Robbins A, Schwartz-Giblin S, Pfaff DW (1987) Ascending and descending projections to medullary reticular sites which activate epaxial muscles in the rat. Soc Neurosci Abstracts 13: 59 (Abstract 21.3)Google Scholar
  76. Robbins A, Schwartz-Giblin S, Pfaff DW (1988) Reticulo-reticular and reticulo-spinal connections affecting EMG activity in rat back muscles. Soc Neurosci Abstracts 14: 184 (Abstract 79.11)Google Scholar
  77. Rodriguez-Sierra JF, Crowley WR, Komisaruk BR (1975) Vaginal stimulation in rats induces prolonged lordosis responsiveness and sexual receptivity. J Comp Physiol Psychol 89: 79–85PubMedCrossRefGoogle Scholar
  78. Rothfeld JM, Harlan RE, Shivers BD, Pfaff DW (1986) Reversible disruption of lordosis via midbrain infusions of procaine and tetrodotoxin. Pharmacol Biochem Behav 25: 857–863PubMedCrossRefGoogle Scholar
  79. Russell DH (1983) Microinjection of purified ornithine decarboxylase into Xenopus oocytes selectively stimulates ribosomal RNA synthesis. Proc Natl Acad Sci USA 80: 1318–1321PubMedCrossRefGoogle Scholar
  80. Sakuma Y, Pfaff DW (1979a) Facilitation of female reproductive behavior from mesencephalic central gray in the rat. Am J Physiol 237: R278–R284PubMedGoogle Scholar
  81. Sakuma Y, Pfaff DW (1979b) Mesencephalic mechanisms for integration of female reproductive behavior in the rat. Am J Physiol 237: R285–R290PubMedGoogle Scholar
  82. Sakuma Y, Pfaff DW (1980a) Convergent effects of lordosis-relevant somatosensory and hypothalamic influences on central gray cells in the rat mesencephalon. Exp Neurol 70: 269–281PubMedCrossRefGoogle Scholar
  83. Sakuma Y, Pfaff DW (1980b) Excitability of female rat central gray cells with medullary projections: changes produced by hypothalamic stimulation and estrogen treatment. J Neurophysiol 44: 1012–1023PubMedGoogle Scholar
  84. Sakuma Y, Pfaff DW (1980c) LH-RH in the mesencephalic central grey can potentiate lordosis reflex of female rats. Nature 283: 566–567PubMedCrossRefGoogle Scholar
  85. Sakuma Y, Pfaff DW (1983) Modulation of the lordosis reflex of female rats by LHRH, its antiserum and analogs in the mesencephalic central gray. Neuroendocrinology 36: 218–224PubMedCrossRefGoogle Scholar
  86. Schwartz-Giblin S, Pfaff DW (1980) Implanted strain gauge and EMG amplifier to record motor behavior in unrestrained rats. Physiol Behav 25: 475–479PubMedCrossRefGoogle Scholar
  87. Schwartz-Giblin S, Rosello L, Pfaff DW (1983) A histochemical study of lateral longissimus muscle in rat. Exp Neurol 79: 497–518PubMedCrossRefGoogle Scholar
  88. Schwartz-Giblin S, Femano P, Pfaff DW (1984a) Axial electromyogram and intervertebral length gauge responses during lordosis behavior in rats. Exp Neurol 85: 297–315PubMedCrossRefGoogle Scholar
  89. Schwartz-Giblin S, Halpern M, Pfaff DW (1984b) Segmental organization of rat lateral longissimus, a muscle- involved in lordosis behavior: EMG and muscle nerve recordings. Brain Res 299: 247–257PubMedCrossRefGoogle Scholar
  90. Schwartz-Giblin S, Pfaff DW (1988) Control of amplitude in a cutaneous reflex subserving lordosis: a role for a progesterone metabolite. Soc Neurosci Abstracts 14: 184 (Abstract 79.14)Google Scholar
  91. Shapovalov AI, Gurevitch NR (1970) Monosynaptic and disynaptic reticulospinal actions on lumbar motoneurons of the rat. Brain Res 21: 249–263PubMedCrossRefGoogle Scholar
  92. Soprano KJ, Dev GV, Croce CM, Baserga R (1979) Reactivation of silent rRNA genes by simian virus 40 in human-mouse hybrid cells. Proc Natl Acad Sci USA 76: 3885–3889PubMedCrossRefGoogle Scholar
  93. Sullivan JM, Schwartz-Giblin S, Pfaff DW (1986) Correlations between EEG state and spontaneous and evoked axial muscle EMG. Brain Res 368: 197–200PubMedCrossRefGoogle Scholar
  94. Tjian R, Fey G, Graessmann A (1978) Biological activity of purified simian virus 40 T antigen proteins. Proc Natl Acad Sci USA 75: 1279–1283PubMedCrossRefGoogle Scholar
  95. Torah-Allerand CD (1976) Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: implications for sexual differentiation. Brain Res 106: 407–412CrossRefGoogle Scholar
  96. Yamanouchi K, Arai Y (1985) The role of mesencephalic tegmentum. in regulating female rat sexual behaviors. Physiol Behav 35: 255–259PubMedCrossRefGoogle Scholar
  97. Yamanouchi K, Nakano Y, Fukuda M, Arai Y (1984) Mesencephalic central gray as supraspinal neural substrates for lordosis reflex: deprivation of serotonergic influence by p-chlorophenylalanine. Zool Sci 1: 126–131Google Scholar
  98. Yu W (1982a) Sex difference in the regeneration of hypoglossal nerve. Brain Res 238: 404–406PubMedCrossRefGoogle Scholar
  99. Yu W (1982b) Effect of testosterone on regeneration of hypoglossal nerve. Exp Neurol 77: 129–141PubMedCrossRefGoogle Scholar
  100. Yu W, Yu M (1983) Acceleration of regeneration of crushed hypoglossal nerve by testosterone. Exp Neural 80: 349–360CrossRefGoogle Scholar
  101. Zemlan FP, Pfaff DW (1975) Lordosis after cerebellar damage in female rats. Horm. Behav 6: 27–33PubMedCrossRefGoogle Scholar
  102. Zemlan FP, Pfaff DW (1979) Topographical organization in medullary reticulospinal systems as demonstrated by the horseradish peroxidase technique. Brain Res 174: 161–166PubMedCrossRefGoogle Scholar
  103. Zemlan FP, Leonard CM, Kow LM, Pfaff DW (1978) Ascending tracts of the lateral columns of the rat spinal cord: a study using the silver impregnation and horseradish peroxidase techniques. Exp Neural 62: 298–334CrossRefGoogle Scholar
  104. Zemlan F, Kow L-M, Morrell JI, Pfaff DW (1979) Descending tracts of the lateral columns of the rat spinal cord: a study using the horseradish peroxidase and silver impregnation techniques. J Anat. 128: 489–512PubMedGoogle Scholar
  105. Zemlan FP, Kow L-M, Pfaff DW (1983) Effect of interruption of bulbospinal pathways on lordosis, posture, and locomotion. Exp Neurol 81: 177–194PubMedCrossRefGoogle Scholar
  106. Zemlan FP, Behbehani MM, Beckstead RM (1984) Ascending and descending projections from nucleus reticularis magnocellularis and nucleus reticularis gigantocellularis: an autoradiographic and horseradish peroxidase study in the rat. Brain Res 292: 207–220PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1989

Authors and Affiliations

  • D. W. Pfaff
    • 1
  • A. Robbins
    • 1
  1. 1.Laboratory of Neurobiology and BehaviorThe Rockefeller UniversityNew YorkUSA

Personalised recommendations