Publication Cover
Stress
The International Journal on the Biology of Stress
Volume 15, 2012 - Issue 5
751
Views
28
CrossRef citations to date
0
Altmetric
Original Research Reports

Wistar rats subjected to chronic restraint stress display increased hippocampal spine density paralleled by increased expression levels of synaptic scaffolding proteins

, , , &
Pages 514-523 | Received 02 Mar 2011, Accepted 06 Nov 2011, Published online: 10 Jan 2012

References

  • Alquicer G, Morales-Medina JC, Quirion R, Flores G. 2008. Postweaning social isolation enhances morphological changes in the neonatal ventral hippocampal lesion rat model of psychosis. J Chem Neuroanat. 35:179–187.
  • Andersen CL, Jensen JL, Orntoft TF. 2004. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64:5245–5250.
  • Bartesaghi R, Severi S, Guidi S. 2003. Effects of early environment on pyramidal neuron morphology in field CA1 of the guinea-pig. Neuroscience. 116:715–732.
  • Beck KD, Luine VN. 2002. Sex differences in behavioral and neurochemical profiles after chronic stress: Role of housing conditions. Physiol Behav. 75:661–673.
  • Bonefeld BE, Elfving B, Wegener G. 2008. Reference genes for normalization: A study of rat brain tissue. Synapse. 62:302–309.
  • Brusco J, Wittmann R, de Azevedo MS, Lucion AB, Franci CR, Giovenardi M, Rasia-Filho AA. 2008. Plasma hormonal profiles and dendritic spine density and morphology in the hippocampal CA1 stratum radiatum, evidenced by light microscopy, of virgin and postpartum female rats. Neurosci Lett. 438:346–350.
  • Campana AD, Sanchez F, Gamboa C, Gomez-Villalobos Mde J, De La Cruz F, Zamudio S, Flores G. 2008. Dendritic morphology on neurons from prefrontal cortex, hippocampus, and nucleus accumbens is altered in adult male mice exposed to repeated low dose of malathion. Synapse. 62:283–290.
  • Cook SC, Wellman CL. 2004. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol. 60:236–248.
  • Critchlow HM, Maycox PR, Skepper JN, Krylova O. 2006. Clozapine and haloperidol differentially regulate dendritic spine formation and synaptogenesis in rat hippocampal neurons. Mol Cell Neurosci. 32:356–365.
  • Czeh B, Lucassen PJ. 2007. What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated?. Eur Arch Psychiatry Clin Neurosci. 257:250–260.
  • Dalla C, Whetstone AS, Hodes GE, Shors TJ. 2009. Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females. Neurosci Lett. 449:52–56.
  • Donohue HS, Gabbott PL, Davies HA, Rodriguez JJ, Cordero MI, Sandi C, Medvedev NI, Popov VI, Colyer FM, Peddie CJ, Stewart MG. 2006. Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: A stereological and three-dimensional ultrastructural study. Neuroscience. 140:597–606.
  • Elfving B, Bonefeld BE, Rosenberg R, Wegener G. 2008. Differential expression of synaptic vesicle proteins after repeated electroconvulsive seizures in rat frontal cortex and hippocampus. Synapse. 62:662–670.
  • Feng J, Yan Z, Ferreira A, Tomizawa K, Liauw JA, Zhuo M, Allen PB, Ouimet CC, Greengard P. 2000. Spinophilin regulates the formation and function of dendritic spines. Proc Natl Acad Sci USA. 97:9287–9292.
  • Garrett JE, Wellman CL. 2009. Chronic stress effects on dendritic morphology in medial prefrontal cortex: Sex differences and estrogen dependence. Neuroscience. 162:195–207.
  • Gibb R, Kolb B. 1998. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods. 79:1–4.
  • Gonzalez CL, Kolb B. 2003. A comparison of different models of stroke on behaviour and brain morphology. Eur J Neurosci. 18:1950–1962.
  • Hageman I, Nielsen M, Wortwein G, Diemer NH, Jorgensen MB. 2008. Electroconvulsive stimulations prevent stress-induced morphological changes in the hippocampus. Stress. 11:282–289.
  • Hageman I, Nielsen M, Wortwein G, Diemer NH, Jorgensen MB. 2009. Electroconvulsive stimulations normalizes stress-induced changes in the glucocorticoid receptor and behaviour. Behav Brain Res. 196:71–77.
  • Kirov SA, Harris KM. 1999. Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated. Nat Neurosci. 2:878–883.
  • Komatsuzaki Y, Murakami G, Tsurugizawa T, Mukai H, Tanabe N, Mitsuhashi K, Kawata M, Kimoto T, Ooishi Y, Kawato S. 2005. Rapid spinogenesis of pyramidal neurons induced by activation of glucocorticoid receptors in adult male rat hippocampus. Biochem Biophys Res Commun. 335:1002–1007.
  • Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E. 2011. Stress revisited: A critical evaluation of the stress concept. Neurosci Biobehav Rev. 35:1291–1301.
  • Luine V, Martinez C, Villegas M, Magarinos AM, McEwen BS. 1996. Restraint stress reversibly enhances spatial memory performance. Physiol Behav. 59:27–32.
  • Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience. 1995a; 69:89–98.
  • Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Comparison of stressors. Neuroscience. 1995b; 69:83–88.
  • Magarinos AM, Li CJ, Toth JG, Bath KG, Jing D, Lee FS, McEwen BS. 2011. Effect of brain-derived neurotrophic factor haploinsufficiency on stress-induced remodeling of hippocampal neurons. Hippocampus. 21:253–264.
  • Martinez-Tellez RI, Hernandez-Torres E, Gamboa C, Flores G. 2009. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse. 63:794–804.
  • McEwen BS. 1999. Stress and hippocampal plasticity. Annu Rev Neurosci. 22:105–122.
  • McEwen BS. 2006. Protective and damaging effects of stress mediators: Central role of the brain. Dialogues Clin Neurosci. 8:367–381.
  • McEwen BS. 2008. Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol. 583:174–185.
  • McEwen BS, Gianaros PJ. 2011. Stress- and allostasis-induced brain plasticity. Annu Rev Med. 62:431–445.
  • McEwen BS, Wingfield JC. 2010. What is in a name? Integrating homeostasis, allostasis and stress. Horm Behav. 57:105–111.
  • McLaughlin KJ, Baran SE, Wright RL, Conrad CD. 2005. Chronic stress enhances spatial memory in ovariectomized female rats despite CA3 dendritic retraction: Possible involvement of CA1 neurons. Neuroscience. 135:1045–1054.
  • McLaughlin KJ, Gomez JL, Baran SE, Conrad CD. 2007. The effects of chronic stress on hippocampal morphology and function: An evaluation of chronic restraint paradigms. Brain Res. 1161:56–64.
  • McLaughlin KJ, Wilson JO, Harman J, Wright RL, Wieczorek L, Gomez J, Korol DL, Conrad CD. 2010. Chronic 17beta-estradiol or cholesterol prevents stress-induced hippocampal CA3 dendritic retraction in ovariectomized female rats: Possible correspondence between CA1 spine properties and spatial acquisition. Hippocampus. 20:768–786.
  • Milosevic NT, Ristanovic D. 2007. The Sholl analysis of neuronal cell images: Semi-log or log-log method?. J Theor Biol. 245:130–140.
  • Monroy E, Hernandez-Torres E, Flores G. 2010. Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. J Chem Neuroanat. 40:93–101.
  • Orlowski D, Bjarkam CR. 2009. Autometallographic enhancement of the Golgi-Cox staining enables high resolution visualization of dendrites and spines. Histochem Cell Biol. 132:369–374.
  • Orlowski D, Soltys Z, Janeczko K. 2003. Morphological development of microglia in the postnatal rat brain. A quantitative study. Int J Dev Neurosci. 21:445–450.
  • Parihar VK, Hattiangady B, Kuruba R, Shuai B, Shetty AK. 2011. Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory. Mol Psychiatry. 16:171–183.
  • Pham K, Nacher J, Hof PR, McEwen BS. 2003. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci. 17:879–886.
  • Ristanovic D, Nedeljkov V, Stefanovic BD, Milosevic NT, Grgurevic M, Stulic V. 2002. Fractal and nonfractal analysis of cell images: Comparison and application to neuronal dendritic arborization. Biol Cybern. 87:278–288.
  • Sala C, Piech V, Wilson NR, Passafaro M, Liu G, Sheng M. 2001. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron. 31:115–130.
  • Sarrouilhe D, di Tommaso A, Metaye T, Ladeveze V. 2006. Spinophilin: From partners to functions. Biochimie. 88:1099–1113.
  • Shi SH, Cox DN, Wang D, Jan LY, Jan YN. 2004. Control of dendrite arborization by an Ig family member, dendrite arborization and synapse maturation 1 (Dasm1). Proc Natl Acad Sci USA. 101:13341–13345.
  • Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat. 87:387–406.
  • Shors TJ, Falduto J, Leuner B. 2004. The opposite effects of stress on dendritic spines in male vs. female rats are NMDA receptor-dependent. Eur J Neurosci. 19:145–150.
  • Smith TGJr, Marks WB, Lange GD, Sheriff WHJr, Neale EA. 1989. A fractal analysis of cell images. J Neurosci Methods. 27:173–180.
  • Sunanda, Meti BL, Raju TR. 1997. Entorhinal cortex lesioning protects hippocampal CA3 neurons from stress-induced damage. Brain Res. 770:302–306.
  • Tata DA, Anderson BJ. 2010. The effects of chronic glucocorticoid exposure on dendritic length, synapse numbers and glial volume in animal models: Implications for hippocampal volume reductions in depression. Physiol Behav. 99:186–193.
  • Toth E, Gersner R, Wilf-Yarkoni A, Raizel H, Dar D, Richter-Levin G, Levit O, Zangen A. 2008. Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J Neurochem. 107:522–532.
  • Vestergaard-Poulsen P, Wegener G, Hansen B, Bjarkam CR, Blackband SJ, Nielsen NC, Jespersen SN. 2011. Diffusion-weighted MRI and quantitative biophysical modeling of hippocampal neurite loss in chronic stress. PLoS ONE. 6:e20653.
  • Watanabe Y, Gould E, McEwen BS. 1992. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588:341–345.
  • Woolley CS, Gould E, McEwen BS. 1990. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531:225–231.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.