Top

Published in:

01-01-2011 | Original Article

Estradiol reduces dendritic spine density in the ventral striatum of female Syrian hamsters

Authors: Nancy A. Staffend, Caroline M. Loftus, Robert L. Meisel

Published in: Brain Structure and Function | Issue 3-4/2011

Abstract

Estradiol affects a variety of brain regions by modulating physiological and cellular functions as well as neuronal morphology. Within the striatum, estradiol is known to induce physiological and molecular changes, yet estradiol’s effects on striatal dendritic morphology have not yet been evaluated. Using ballistic delivery of the lipophilic dye DiI to tissue sections, we were able to evaluate estradiol’s effects on striatal morphology in female Syrian hamsters. We found that estradiol significantly decreased spine density within the nucleus accumbens core, with no effect in the nucleus accumbens shell or caudate. Interestingly, estradiol treatment caused a significant deconstruction of spines from more to less mature spine subtypes in both the nucleus accumbens core and shell regardless of changes in spine density. These results are significant in that they offer a novel mechanism for estradiol actions on a wide variety of nucleus accumbens functions such as motivation or reward as well as their pathological consequences (e.g. drug addiction).

Anwyl R (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29:83–120CrossRefPubMed

Becker JB (2000) Oestrogen effects on dopaminergic function in striatum. Novartis Found Symp 230:134–145; discussion 145–154

Becker JB, Hu M (2008) Sex differences in drug abuse. Front Neuroendocrinol 29:36–47CrossRefPubMed

Bourque M, Dluzen DE, Di Paolo T (2009) Neuroprotective actions of sex steroids in Parkinson’s disease. Front Neuroendocrinol 30:142–157CrossRefPubMed

Bradley KC, Haas AR, Meisel RL (2005) 6-Hydroxydopamine lesions in female hamsters (Mesocricetus auratus) abolish the sensitized effects of sexual experience on copulatory interactions with males. Behav Neurosci 119:224–232CrossRefPubMed

Calizo LH, Flanagan-Cato LM (2000) Estrogen selectively regulates spine density within the dendritic arbor of rat ventromedial hypothalamic neurons. J Neurosci 20:1589–1596PubMed

Calizo LH, Flanagan-Cato LM (2002) Estrogen-induced dendritic spine elimination on female rat ventromedial hypothalamic neurons that project to the periaqueductal gray. J Comp Neurol 447:234–248CrossRefPubMed

Chen JC, Chen PC, Chiang YC (2009) Molecular mechanisms of psychostimulant addiction. Chang Gung Med J 32:148–154PubMed

Cooke BM, Woolley CS (2005) Gonadal hormone modulation of dendrites in the mammalian CNS. J Neurobiol 64:34–46CrossRefPubMed

Cyr M, Calon F, Morissette M, Di Paolo T (2002) Estrogenic modulation of brain activity: implications for schizophrenia and Parkinson’s disease. J Psychiatry Neurosci 27:12–27PubMed

de Castilhos J, Forti CD, Achaval M, Rasia-Filho AA (2008) Dendritic spine density of posterodorsal medial amygdala neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: a Golgi study. Brain Res 1240:73–81CrossRefPubMed

Donahue JE, Stopa EG, Chorsky RL, King JC, Schipper HM, Tobet SA, Blaustein JD, Reichlin S (2000) Cells containing immunoreactive estrogen receptor-alpha in the human basal forebrain. Brain Res 856:142–151CrossRefPubMed

Ferraguti F, Shigemoto R (2006) Metabotropic glutamate receptors. Cell Tissue Res 326:483–504CrossRefPubMed

Frankfurt M, Gould E, Woolley CS, McEwen BS (1990) Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: a Golgi study in the adult rat. Neuroendocrinology 51:530–535CrossRefPubMed

Gan WB, Grutzendler J, Wong WT, Wong RO, Lichtman JW (2000) Multicolor “DiOlistic” labeling of the nervous system using lipophilic dye combinations. Neuron 27:219–225CrossRefPubMed

Gan WB, Grutzendler J, Wong RO, Lichtman JW (2009) Ballistic delivery of dyes for structural and functional studies of the nervous system. Cold Spring Harb Protoc (pdb.prot5202)

Grove-Strawser D, Boulware MI, Mermelstein PG (2010) Membrane estrogen receptors activate the metabotropic glutamate receptors mGluR5 and mGluR3 to bidirectionally regulate CREB phosphorylation in female rat striatal neurons. Neuroscience 140:1045–1055

Hao J, Rapp PR, Leffler AE, Leffler SR, Janssen WG, Lou W, McKay H, Roberts JA, Wearne SL, Hof PR, Morrison JH (2006) Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci 26:2571–2578CrossRefPubMed

Harris KM, Jensen FE, Tsao B (1992) Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12:2685–2705PubMed

Hedges VL, Chakravarty S, Nestler EJ, Meisel RL (2009) Delta FosB overexpression in the nucleus accumbens enhances sexual reward in female Syrian hamsters. Genes Brain Behav 8:442–449CrossRefPubMed

Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2:880–888CrossRefPubMed

Kelley AE, Domesick VB (1982) The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde- and retrograde-horseradish peroxidase study. Neuroscience 7:2321–2335CrossRefPubMed

Korol DL (2004) Role of estrogen in balancing contributions from multiple memory systems. Neurobiol Learn Mem 82:309–323CrossRefPubMed

Kourrich S, Rothwell PE, Klug JR, Thomas MJ (2007) Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J Neurosci 27:7921–7928CrossRefPubMed

McEwen B (2002) Estrogen actions throughout the brain. Recent Prog Horm Res 57:357–384CrossRefPubMed

McKinney RA, Capogna M, Durr R, Gahwiler BH, Thompson SM (1999) Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 2:44–49CrossRefPubMed

Meisel RL, Mullins AJ (2006) Sexual experience in female rodents: cellular mechanisms and functional consequences. Brain Res 1126:56–65CrossRefPubMed

Meredith GE, Agolia R, Arts MP, Groenewegen HJ, Zahm DS (1992) Morphological differences between projection neurons of the core and shell in the nucleus accumbens of the rat. Neuroscience 50:149–162CrossRefPubMed

Mermelstein PG, Becker JB, Surmeier DJ (1996) Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. J Neurosci 16:595–604PubMed

Morissette M, Le Saux M, D’Astous M, Jourdain S, Al Sweidi S, Morin N, Estrada-Camarena E, Mendez P, Garcia-Segura LM, Di Paolo T (2008) Contribution of estrogen receptors alpha and beta to the effects of estradiol in the brain. J Steroid Biochem Mol Biol 108:327–338CrossRefPubMed

Mukai H, Tsurugizawa T, Murakami G, Kominami S, Ishii H, Ogiue-Ikeda M, Takata N, Tanabe N, Furukawa A, Hojo Y, Ooishi Y, Morrison JH, Janssen WG, Rose JA, Chambon P, Kato S, Izumi S, Yamazaki T, Kimoto T, Kawato S (2007) Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J Neurochem 100:950–967CrossRefPubMed

O’Brien JA, Holt M, Whiteside G, Lummis SC, Hastings MH (2001) Modifications to the hand-held Gene Gun: improvements for in vitro biolistic transfection of organotypic neuronal tissue. J Neurosci Methods 112:57–64CrossRefPubMed

O’Donnell P, Grace AA (1995) Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci 15:3622–3639PubMed

Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47(Suppl 1):33–46CrossRefPubMed

Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858–5867PubMed

Schoepp DD (2001) Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system. J Pharmacol Exp Ther 299:12–20PubMed

Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213–242CrossRefPubMed

Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168:3–20CrossRef

Shen HW, Toda S, Moussawi K, Bouknight A, Zahm DS, Kalivas PW (2009) Altered dendritic spine plasticity in cocaine-withdrawn rats. J Neurosci 29:2876–2884CrossRefPubMed

Skynner MJ, Sim JA, Herbison AE (1999) Detection of estrogen receptor alpha and beta messenger ribonucleic acids in adult gonadotropin-releasing hormone neurons. Endocrinology 140:5195–5201CrossRefPubMed

Szego EM, Kekesi KA, Szabo Z, Janaky T, Juhasz GD (2010) Estrogen regulates cytoskeletal flexibility, cellular metabolism and synaptic proteins: a proteomic study. Psychoneuroendocrinology 35:807–819CrossRefPubMed

Tamaru Y, Nomura S, Mizuno N, Shigemoto R (2001) Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106:481–503CrossRefPubMed

Tunez I, Collado JA, Medina FJ, Pena J, Del CMM, Jimena I, Franco F, Rueda I, Feijoo M, Muntane J, Montilla P (2006) 17 beta-Estradiol may affect vulnerability of striatum in a 3-nitropropionic acid-induced experimental model of Huntington’s disease in ovariectomized rats. Neurochem Int 48:367–373CrossRefPubMed

Walf AA, Frye CA (2008) Rapid and estrogen receptor beta mediated actions in the hippocampus mediate some functional effects of estrogen. Steroids 73:997–1007CrossRefPubMed

Wang XB, Zhou Q (2010) Spine remodeling and synaptic modification. Mol Neurobiol 41:29–41CrossRefPubMed

Woolley CS (1998) Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 34:140–148CrossRefPubMed

Woolley CS, Cohen RS (2002) Sex steroids and neuronal growth in adulthood. In: Pfaff DW, Arnold AA, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones brain and behavior, vol 4. Elsevier Science, San Diego, pp 717–777

Woolley CS, McEwen BS (1993) Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293–306CrossRefPubMed

Woolley CS, Gould E, Frankfurt M, McEwen BS (1990) Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035–4039PubMed

Title: Estradiol reduces dendritic spine density in the ventral striatum of female Syrian hamsters
Authors: Nancy A. Staffend
Caroline M. Loftus
Robert L. Meisel
Publication date: 01-01-2011
Publisher: Springer-Verlag
Published in: Brain Structure and Function / Issue 3-4/2011
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-010-0284-7

At a glance: The STEP trials

Springer Medicine

Estradiol reduces dendritic spine density in the ventral striatum of female Syrian hamsters

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3-4/2011

ALE meta-analysis on facial judgments of trustworthiness and attractiveness

Projections from the brain to the spinal cord in the mouse

Sex differences in cognitive control are associated with midcingulate and callosal morphology

3D global and regional patterns of human fetal subplate growth determined in utero

Prominent periventricular fiber system related to ganglionic eminence and striatum in the human fetal cerebrum

Atrophy in the parahippocampal gyrus as an early biomarker of Alzheimer’s disease