Skip to main content
Log in

Estrogen-induced alterations in synaptic morphology in the midbrain central gray

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Axons of ventromedial hypothalamic (VMH) neurons have been previously shown to terminate in the midbrain central gray (MCG) (Chung et al. 1984, 1986). Since VMH synapses in this region may be involved in the mediation of estrogen-induced lordosis behavior, we examined the effect of estrogen on the morphology of synapses in the MCG. Ovariectomized adult female rats were given daily subcutaneous injections of estradiol benzoate (10 μg) or the vehicle control and after 20 days of injection, only the estrogen-treated rats showed the lordosis response. A quantitative analysis of MCG tissue from these animals demonstrates morphological changes in various synaptic parameters with estrogen treatment including: 1) an increase in the mean number of dense-cored vesicles and an increase in the number of terminals containing densecored vesicles, 2) an increase in the length of postsynaptic densities (PSDs), 3) an increase in the number of PSDs showing perforations, 4) an increase in the number of synapses, and 5) an increase in the number of synapses with positive synaptic curvature. No alterations in the number of subjunctional bodies were observed. The dense-cored vesicles may contain an estrogen-induced trophic factor which may function in maintaining the integrity of postsynaptic processes and cells in the MCG with which VMN endings contact (Chung et al. submitted) and/or which induces morphological changes in postsynaptic structures which facilitate the effects of estrogen on lordosis behavior.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akert K (1973) Dynamic aspects of synaptic ultrastructure. Brain Res 49: 511–518

    Google Scholar 

  • Artyukhina NI, Ryabinina MA (1980) Ultrastructural changes in synapses of the rabbit sensomotor cortex during stimulation of the reticular formation. Neurosci Behav Physiol 10(5): 438–445

    Google Scholar 

  • Bailey CH, Chen M (1983) Morphological basis of long-term habituation and sensitization in Aplysia. Science 220: 91–93

    Google Scholar 

  • Beach FA, Orndoff RK (1974) Variation in the responsiveness of female rats to ovarian hormones as a function of preceding hormonal deprivation. Horm Behav 5: 202–205

    Google Scholar 

  • Carlin RK, Grab DJ, Cohen RS, Siekevitz P (1980) Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 86: 831–843

    Google Scholar 

  • Carlin RK, Siekevitz P (1983) Plasticity in the central nervous system: do synapses divide? Proc Natl Acad Sci USA 80: 3517–3521

    Google Scholar 

  • Carrer HF, Aoki A (1982) Ultrastructural changes in the hypothalamic ventromedial nucleus of ovariectomized rats after estrogen treatment. Brain Res 240: 221–233

    Google Scholar 

  • Chung SK, Pfaff DW, Cohen RS (1984) Projections of ventromedial hypothalamic neurons to the midbrain central gray: an ultrastructural study. Soc Neurosci Abstr 10(1): 210

    Google Scholar 

  • Chung SK, Pfaff DW, Cohen RS (1986) Transsynaptic degeneration in midbrain central gray after VMN lesions: a qualitative and quantitative analysis. Soc Neurosci Abstr 12(1): 606

    Google Scholar 

  • Cohen RS, Chung SK, Pfaff DW (1984) Alteration by estrogen of the nucleoli in nerve cells of the rat hypothalamus. Cell Tissue Res 235: 485–489

    Google Scholar 

  • Cohen RS, 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: 451–470

    Google Scholar 

  • Cohen RS, Pfaff DW (1985) Cell biological and math-logical theories of the neural circuit for steroid-dependent female reproductive behavior. Integrative Psychiatry 3: 262–279

    Google Scholar 

  • DeVoogd TJ, Nixdorf B, Nottebohm F (1982) Recruitment of additional synapses into a brain network takes extra brain space. Soc Neurosci Abstr 8(12): 141

    Google Scholar 

  • Dyson SE, Jones DG (1980) Quantitation of terminal parameters and their interrelationships in maturing central synapses: a perspective for experimental studies. Brain Res 183: 43–59

    Google Scholar 

  • Gerall AA, Dunlap JL (1973) The effect of experience and hormones on the initial receptivity in female and male rats. Physiol Behav 10: 851–854

    Google Scholar 

  • Greene R, Luttge WG, Whalen RE (1970) Induction of receptivity in ovariectomized female rats by a single intravenous injection of estradiol-17β. Physiol Behav 5: 137–141

    Google Scholar 

  • Greenough W, West RW, DeVoogd TJ (1978) Subsynaptic plate perforations: changes with age and experience in the rat. Science 202: 1096–1098

    Google Scholar 

  • Güldner FH, Ingham CA (1979) Plasticity in synaptic appositions of optic nerve afferents under different lighting conditions. Neurosci Lett 14: 235–240

    Google Scholar 

  • Harlan RE, Shivers BD, Kow L-M, Pfaff DW (1982) Intrahypothalamic colchicine infusions disrupt lordotic responsiveness in estrogen-treated female rats. Brain Res 238: 153–167

    Google Scholar 

  • Hatton JD, Ellisman MH (1982) A restructuring of hypothalamic synapses is associated with motherhood. J Neurosci 2: 704–707

    Google Scholar 

  • Jones DG, Devon RM (1978) An ultrastructural study into the effects of pentobarbitone on synaptic organization. Brain Res 147: 47–63

    Google Scholar 

  • Jones KJ, Chikaraishi DM, Harrington CA, McEwen B, Pfaff DW (1986) In situ hybridization detection of estradiol-induced changes in ribosomal RNA levels in rat brain. Molec Brain Res 387(2): 153–166

    Google Scholar 

  • Jones KJ, Pfaff DW, McEwen B (1985) Early estrogen-induced nuclear changes in rat hypothalamic ventromedial neurons: an ultrastructural and morphometric analysis. J Comp Neurol 239: 255–266

    Google Scholar 

  • König JFR, Klippel RA (1963) The rat brain. A stereotaxic atlas of the forebrain and lower parts of the brainstem. Williams and Wilkins, Baltimore, Maryland

    Google Scholar 

  • 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: 197–205

    CAS  PubMed  Google Scholar 

  • McEwen BS, Pfaff DW, Chaptal C, Luine V (1975) Brain cell nuclear retention of [3H]estradiol doses able to promote lordosis: temporal and regional aspects. Brain Res 86: 155–161

    Google Scholar 

  • Medosch CM, Diamond MC (1982) Rat occipital cortical synapses after ovariectomy. Exp Neurol 75: 120–133

    Google Scholar 

  • Meisel RL, Pfaff DW (1983) Protein synthesis and the regulation of sexual behavior and neuronal ultrastructure by estrogen in the female rat. Soc Neurosci Abstr 9(2): 1078

    Google Scholar 

  • Meisel RL, Pfaff DW (1985a) Specificity and neural sites of action of anisomycin in the reduction or facilitation of female sexual behavior in rats. Horm Behav 19: 237–251

    Google Scholar 

  • Meisel RL, Pfaff DW (1985b) Brain region specificity in estradiol effects on neuronal ultrastructure in rats. Mol Cell Endocrinol 40: 159–166

    Google Scholar 

  • Milhaud M, Pappas GD (1986) The fine structure of neurons and synapses of the habenula of the cat with special reference to subjunctional bodies. Brain Res 3: 158–173

    Google Scholar 

  • Mobbs CV, Harlen RE, Pfaff DW (1985) An estradiol-induced protein synthesized in the ventral medial hypothalamus (VMH) and transported to the midbrain central gray (MCG). Soc Neurosci Abstr 11(2): 1271

    Google Scholar 

  • Møllgaard K, Diamond MC, Bennett EL, Rosenzweig MR, Lindner B (1971) Quantitative synaptic changes with differential experience in rat brain. Int J Neurosci 2: 113–127

    Google Scholar 

  • Nieto-Sampedro M, Hoff SF, Cotman CW (1982) Perforated postsynaptic densities: probable intermediates in synaptic turnover. Proc Natl Acad Sci USA 79: 5718–5722

    Google Scholar 

  • Parsons B, MacLusky NJ, Krieger MS, McEwen BS, Pfaff DW (1979) The effects of long-term estrogen exposure on the induction of sexual behavior and measurements of brain estrogen and progestin receptors in the female rat. Horm Behav 13: 301–313

    Google Scholar 

  • Peters A, Kaiserman-Abramof IR (1968) The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Z Mikrosk Anat Forsch 100: 487–506

    Google Scholar 

  • Pfaff DW (1980) Estrogens and brain function. Springer, New York

    Google Scholar 

  • Pfaff DW (1983) Impact of estrogens on hypothalamic nerve cells: ultrastructural, chemical and electrical effects. Rec Prog Horm Res 39: 127–179

    Google Scholar 

  • Pfaff DW (1987) Gene expression of behaviorally relevant peptides in hypothalamic neurons. Prog Brain Res 72: 129–136

    Google Scholar 

  • Pfaff DW, Cohen RS (1987) Estrogen acting on hypothalamic neurons may have trophic effects on those neurons and the cells on which they synapse. In: Leung PCK, Armstrong DT, Ruf KB, Moger WH, Friesen HG (eds) Endocrinology and physiology of reproduction. Plenum Press, New York, pp 1–11

    Google Scholar 

  • Pfaff DW, Rosello L, Blackburn P (1984) Proteins synthesized in medial hypothalamus and transported to midbrain in estrogen-treated female rats. Exp Brain Res 57(84): 204–207

    Google Scholar 

  • Quadagno DM, Shryne J, Gorski RA (1971) The inhibition of steroid induced sexual behavior by intrahypothalamic actinomycin D. Horm Behav 2: 1–10

    Google Scholar 

  • Rainbow TC, Davis PG, McEwen BS (1980) Anisomycin inhibits the activation of sexual behavior by estradiol and progesterone. Brain Res 194: 548–555

    Google Scholar 

  • Rutledge LT (1978) Effects of cortical denervation and stimulation on axons, dendrites and synapses. In: Cotman CW (ed) Neuronal plasticity. Raven Press, New York, pp 273–289

    Google Scholar 

  • Siekevitz P (1985) The postsynaptic density: a possible role in long-lasting effects in the central nervous system. Proc Natl Acad Sci 82: 3494–3498

    Google Scholar 

  • Terkel AS, Shryne J, Gorski RA (1973) Inhibition of estrogen facilitation of sexual behavior by the intracerebral infusion of actinomycin D. Horm Behav 4: 377–391

    Google Scholar 

  • Tweedle CD, Hatton GI (1982) Magnocellular neuropeptidergic terminals in neurohypophysis: rapid glial release of enclosed axons during parturition. Brain Res Bull 8: 205–209

    Google Scholar 

  • Wesa JM, Change FF, Greenough WT, West RW (1982) Synaptic contact curvature: effects of differential rearing on rat occipital cortex. Develop Brain Res 4: 253–257

    Google Scholar 

  • West RW, Greenough WT (1972) Effect of environmental complexity on cortical synapses of rats: preliminary results. Behav Biol 7: 279–284

    Google Scholar 

  • Whalen RE, Nakayama K (1965) Induction of oestrous behavior: facilitation by repeated hormone treatments. Endocrinology 33: 525–526

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chung, S.K., Pfaff, D.W. & Cohen, R.S. Estrogen-induced alterations in synaptic morphology in the midbrain central gray. Exp Brain Res 69, 522–530 (1988). https://doi.org/10.1007/BF00247306

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00247306

Key words

Navigation