Abstract
Following stress, GMV has been determined using high-resolution MRI for the ACC, hippocampus, amygdala and RSG (Fig. 2.1a–d). Significant volume changes are observed in the ACC of hippocampus but not in the amygdala nor the RSG (Table 2.1).
Reprinted from Mol. Neurobiol. Kassem MS, Lagopoulos J, Stait-Gardner T, Price WS, Chohan TW, Arnold JC, Hatton SN, Bennett MR. Stress-induced grey matter loss determined by MRI is primarily due to loss of dendrites and their synapses . Vol. 47(2):645–661 Copyright (2013). With permission from Springer.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alpar A, Ueberham U, Bruckner MK, Seeger G, Arendt T, Gartner U (2006) Different dendrite and dendritic spine alterations in basal and apical arbors in mutant human amyloid precursor protein transgenic mice. Brain Res 1099(1):189–198. https://doi.org/10.1016/j.brainres.2006.04.109
Balu DT, Basu AC, Corradi JP, Cacace AM, Coyle JT (2012) The NMDA receptor co-agonists, D-serine and glycine, regulate neuronal dendritic architecture in the somatosensory cortex. Neurobiol Dis 45(2):671–682. https://doi.org/10.1016/j.nbd.2011.10.006
Banasr M, Valentine GW, Li XY, Gourley SL, Taylor JR, Duman RS (2007) Chronic unpredictable stress decreases cell proliferation in the cerebral cortex of the adult rat. Biol Psychiatry 62(5):496–504. https://doi.org/10.1016/j.biopsych.2007.02.006
Bannister NJ, Larkman AU (1995) Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: II. Spine distributions. J Comp Neurol 360(1):161–171. https://doi.org/10.1002/cne.903600112
Bell MA, Ball MJ (1985) Laminar variation in the microvascular architecture of normal human visual cortex (area 17). Brain Res 335(1):139–143
Benes FM, Parks TN, Rubel EW (1977) Rapid dendritic atrophy following deafferentation: an EM morphometric analysis. Brain Res 122(1):1–13
Bennett MR (2011) The prefrontal-limbic network in depression: a core pathology of synapse regression. Prog Neurobiol 93(4):457–467. https://doi.org/10.1016/j.pneurobio.2011.01.001
Bennur S, Shankaranarayana Rao BS, Pawlak R, Strickland S, McEwen BS, Chattarji S (2007) Stress-induced spine loss in the medial amygdala is mediated by tissue-plasminogen activator. Neuroscience 144(1):8–16. https://doi.org/10.1016/j.neuroscience.2006.08.075
Blinkov SM, Glezer II (1968) The human brain in figures and tables; a quantitative handbook. Basic Books, New York
Bolstad I, Leergaard TB, Bjaalie JG (2007) Branching of individual somatosensory cerebropontine axons in rat: evidence of divergence. Brain Struct Funct 212(1):85–93. https://doi.org/10.1007/s00429-007-0145-1
Braitenberg V, Schuz A (1998) Cortex: statistics and geometry of neuronal connectivity, 2nd edn. Springer, Berlin
Chen JR, Wang TJ, Huang HY, Chen LJ, Huang YS, Wang YJ, Tseng GF (2009) Fatigue reversibly reduced cortical and hippocampal dendritic spines concurrent with compromise of motor endurance and spatial memory. Neuroscience 161(4):1104–1113. https://doi.org/10.1016/j.neuroscience.2009.04.022
Chen Y, Rex CS, Rice CJ, Dube CM, Gall CM, Lynch G, Baram TZ (2010) Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling. Proc Natl Acad Sci USA 107(29):13123–13128. https://doi.org/10.1073/pnas.1003825107
Conrad CD, LeDoux JE, Magarinos AM, McEwen BS (1999) Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113(5):902–913
Cook SC, Wellman CL (2004) Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60(2):236–248. https://doi.org/10.1002/neu.20025
Cragg BG (1967) The density of synapses and neurones in the motor and visual areas of the cerebral cortex. J Anat 101(Pt 4):639–654
D’Ambrosio R, Wenzel J, Schwartzkroin PA, McKhann GM 2nd, Janigro D (1998) Functional specialization and topographic segregation of hippocampal astrocytes. J Neurosci 18(12):4425–4438
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(1):52–56. https://doi.org/10.1016/j.neulet.2008.10.051
Deitch JS, Rubel EW (1989a) Changes in neuronal cell bodies in N. laminaris during deafferentation-induced dendritic atrophy. J Comp Neurol 281(2):259–268. https://doi.org/10.1002/cne.902810208
Deitch JS, Rubel EW (1989b) Rapid changes in ultrastructure during deafferentation-induced dendritic atrophy. J Comp Neurol 281(2):234–258. https://doi.org/10.1002/cne.902810207
Englisch HJ, Kunz G, Wenzel J (1974) Distribution of spines on the pyramidal neurons in the CA-1 region of the hippocampus in the rat. Z Mikrosk Anat Forsch 88(1):85–102
Foh E, Haug H, Konig M, Rast A (1973) Determination of quantitative parameters of the fine structure in the visual cortex of the cat, also a methodological contribution on measuring the neuropil (author’s transl). Microsc Acta 75(2):148–168
Frotscher M, Nitsch C, Hassler R (1981) Synaptic reorganization in the rabbit hippocampus after lesion of commissural afferents. Anat Embryol (Berl) 163(1):15–30
Griph S, Westman J (1977) Volume composition of the lateral cervical nucleus in the cat. I. A stereological and electron microscopical study of normal and deafferentated animals. J Neurocytol 6(6):723–743
Hama K, Arii T, Katayama E, Marton M, Ellisman MH (2004) Tri-dimensional morphometric analysis of astrocytic processes with high voltage electron microscopy of thick Golgi preparations. J Neurocytol 33(3):277–285. https://doi.org/10.1023/B:NEUR.0000044189.08240.a2
Hamidi M, Drevets WC, Price JL (2004) Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biol Psychiatry 55(6):563–569. https://doi.org/10.1016/j.biopsych.2003.11.006
Hamori J (1990) Morphological plasticity of postsynaptic neurones in reactive synaptogenesis. J Exp Biol 153:251–260
Hill MN, Hillard CJ, McEwen BS (2011) Alterations in corticolimbic dendritic morphology and emotional behavior in cannabinoid CB1 receptor-deficient mice parallel the effects of chronic stress. Cereb Cortex 21(9):2056–2064. https://doi.org/10.1093/cercor/bhq280
Hof PR, Haroutunian V, Friedrich VL Jr, Byne W, Buitron C, Perl DP, Davis KL (2003) Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia. Biol Psychiatry 53(12):1075–1085
Hoff SF (1986) Lesion-induced transneuronal plasticity in the adult rat hippocampus. Neuroscience 19(4):1227–1233
Johnson SA, Wang JF, Sun X, McEwen BS, Chattarji S, Young LT (2009) Lithium treatment prevents stress-induced dendritic remodeling in the rodent amygdala. Neuroscience 163(1):34–39. https://doi.org/10.1016/j.neuroscience.2009.06.005
Kassem MS, Lagopoulos J, Stait-Gardner T, Price WS, Chohan TW, Arnold JC et al (2013) Stress-induced grey matter loss determined by MRI Is primarily due to loss of dendrites and their synapses. Mol Neurobiol 47(2):645–661. https://doi.org/10.1007/s12035-012-8365-7
Knox CA, Oliveira A (1980) Brain aging in normotensive and hypertensive strains of rats. III. A quantitative study of cerebrovasculature. Acta Neuropathol 52(1):17–25
Konur S, Rabinowitz D, Fenstermaker VL, Yuste R (2003) Systematic regulation of spine sizes and densities in pyramidal neurons. J Neurobiol 56(2):95–112. https://doi.org/10.1002/neu.10229
Lehmenkuhler A, Sykova E, Svoboda J, Zilles K, Nicholson C (1993) Extracellular space parameters in the rat neocortex and subcortical white matter during postnatal development determined by diffusion analysis. Neuroscience 55(2):339–351
Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR et al (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26(30):7870–7874. https://doi.org/10.1523/JNEUROSCI.1184-06.2006
Lloyd SA, Wensley B, Faherty CJ, Smeyne RJ (2003) Regional differences in cortical dendrite morphology following in utero exposure to cocaine. Brain Res Dev Brain Res 147(1–2):59–66
Magarinos AM, Li CJ, Gal Toth J, 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(3):253–264. https://doi.org/10.1002/hipo.20744
Marcuzzo S, Dall’oglio A, Ribeiro MF, Achaval M, Rasia-Filho AA (2007) Dendritic spines in the posterodorsal medial amygdala after restraint stress and ageing in rats. Neurosci Lett 424(1):16–21. https://doi.org/10.1016/j.neulet.2007.07.019
Matthews DA, Cotman C, Lynch G (1976) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration. Brain Res 115(1):1–21
Matthews MA, St Onge MF, Faciane CL, Gelderd JB (1979) Spinal cord transection: a quantitative analysis of elements of the connective tissue matrix formed within the site of lesion following administration of piromen, cytoxan or trypsin. Neuropathol Appl Neurobiol 5(3):161–180
McEwen BS (2000a) Effects of adverse experiences for brain structure and function. Biol Psychiatry 48(8):721–731
McEwen BS (2000b) The neurobiology of stress: from serendipity to clinical relevance. Brain Res 886(1–2):172–189
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. https://doi.org/10.1016/j.brainres.2007.05.042
Minkwitz HG, Holz L (1975) The ontogenetic development of pyramidal neurons in the hippocampus (CA1) of the rat. J Hirnforsch 16(1):37–54
Nicholson C, Phillips JM (1981) Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum. J Physiol 321:225–257
Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308(5726):1314–1318. https://doi.org/10.1126/science.1110647
Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F et al (2009) Uniquely hominid features of adult human astrocytes. J Neurosci 29(10):3276–3287. https://doi.org/10.1523/JNEUROSCI.4707-08.2009
Ogata K, Kosaka T (2002) Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113(1):221–233
Pawlak R, Rao BS, Melchor JP, Chattarji S, McEwen B, Strickland S (2005) Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc Natl Acad Sci USA 102(50):18201–18206. https://doi.org/10.1073/pnas.0509232102
Pego JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OF, Sousa N (2008) Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur J Neurosci 27(6):1503–1516. https://doi.org/10.1111/j.1460-9568.2008.06112.x
Pelvig DP, Pakkenberg H, Stark AK, Pakkenberg B (2008) Neocortical glial cell numbers in human brains. Neurobiol Aging 29(11):1754–1762. https://doi.org/10.1016/j.neurobiolaging.2007.04.013
Perez-Cruz C, Muller-Keuker JI, Heilbronner U, Fuchs E, Flugge G (2007) Morphology of pyramidal neurons in the rat prefrontal cortex: lateralized dendritic remodeling by chronic stress. Neural Plast 2007:46276. https://doi.org/10.1155/2007/46276
Pillai AG, de Jong D, Kanatsou S, Krugers H, Knapman A, Heinzmann JM et al (2012) Dendritic morphology of hippocampal and amygdalar neurons in adolescent mice is resilient to genetic differences in stress reactivity. PLoS One 7(6):e38971. https://doi.org/10.1371/journal.pone.0038971
Pokorny J, Yamamoto T (1981) Postnatal ontogenesis of hippocampal CA1 area in rats. II. Development of ultrastructure in stratum lacunosum and moleculare. Brain Res Bull 7(2):121–130
Qin M, Xia Z, Huang T, Smith CB (2011) Effects of chronic immobilization stress on anxiety-like behavior and basolateral amygdala morphology in Fmr1 knockout mice. Neuroscience 194:282–290. https://doi.org/10.1016/j.neuroscience.2011.06.047
Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR et al (2004) Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125(1):1–6. https://doi.org/10.1016/j.neuroscience.2004.01.006
Radley JJ, Rocher AB, Janssen WG, Hof PR, McEwen BS, Morrison JH (2005) Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress. Exp Neurol 196(1):199–203. https://doi.org/10.1016/j.expneurol.2005.07.008
Radley JJ, Rocher AB, Rodriguez A, Ehlenberger DB, Dammann M, McEwen BS, Morrison JH, Wearne SL, Hof PR (2008) Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J Comp Neurol 507(1):1141–1150
Russell FA, Moore DR (1999) Effects of unilateral cochlear removal on dendrites in the gerbil medial superior olivary nucleus. Eur J Neurosci 11(4):1379–1390
Schuz A, Palm G (1989) Density of neurons and synapses in the cerebral cortex of the mouse. J Comp Neurol 286(4):442–455. https://doi.org/10.1002/cne.902860404
Shansky RM, Hamo C, Hof PR, McEwen BS, Morrison JH (2009) Stress-induced dendritic remodeling in the prefrontal cortex is circuit specific. Cereb Cortex 19(10):2479–2484. https://doi.org/10.1093/cercor/bhp003
Somogyi J, Eysel U, Hamori J (1987) A quantitative study of morphological reorganization following chronic optic deafferentation in the adult cat dorsal lateral geniculate nucleus. J Comp Neurol 255(3):341–350. https://doi.org/10.1002/cne.902550303
Sorensen SA, Rubel EW (2006) The level and integrity of synaptic input regulates dendrite structure. J Neurosci 26(5):1539–1550. https://doi.org/10.1523/JNEUROSCI.3807-05.2006
Sousa N, Lukoyanov NV, Madeira MD, Almeida OF, Paula-Barbosa MM (2000) Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97(2):253–266
Spacek J, Hartmann M (1983) Three-dimensional analysis of dendritic spines. I. Quantitative observations related to dendritic spine and synaptic morphology in cerebral and cerebellar cortices. Anat Embryol (Berl) 167(2):289–310
Stepanyants A, Tamas G, Chklovskii DB (2004) Class-specific features of neuronal wiring. Neuron 43(2):251–259. https://doi.org/10.1016/j.neuron.2004.06.013
Stepanyants A, Martinez LM, Ferecsko AS, Kisvarday ZF (2009) The fractions of short- and long-range connections in the visual cortex. Proc Natl Acad Sci USA 106(9):3555–3560. https://doi.org/10.1073/pnas.0810390106
Sykova E, Vorisek I, Antonova T, Mazel T, Meyer-Luehmann M, Jucker M et al (2005a) Changes in extracellular space size and geometry in APP23 transgenic mice: a model of Alzheimer’s disease. Proc Natl Acad Sci USA 102(2):479–484. https://doi.org/10.1073/pnas.0408235102
Sykova E, Vorisek I, Mazel T, Antonova T, Schachner M (2005b) Reduced extracellular space in the brain of tenascin-R- and HNK-1-sulphotransferase deficient mice. Eur J Neurosci 22(8):1873–1880. https://doi.org/10.1111/j.1460-9568.2005.04375.x
Tata DA, Marciano VA, Anderson BJ (2006) Synapse loss from chronically elevated glucocorticoids: relationship to neuropil volume and cell number in hippocampal area CA3. J Comp Neurol 498(3):363–374. https://doi.org/10.1002/cne.21071
Trommald M, Jensen V, Andersen P (1995) Analysis of dendritic spines in rat CA1 pyramidal cells intracellularly filled with a fluorescent dye. J Comp Neurol 353(2):260–274. https://doi.org/10.1002/cne.903530208
Veena J, Srikumar BN, Mahati K, Bhagya V, Raju TR, Shankaranarayana Rao BS (2009) Enriched environment restores hippocampal cell proliferation and ameliorates cognitive deficits in chronically stressed rats. J Neurosci Res 87(4):831–843. https://doi.org/10.1002/jnr.21907
Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22(15):6810–6818. https://doi.org/10.1523/JNEUROSCI.22-15-06810.2002
Vyas A, Bernal S, Chattarji S (2003) Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res 965(1–2):290–294
Vyas A, Pillai AG, Chattarji S (2004) Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128(4):667–673. https://doi.org/10.1016/j.neuroscience.2004.07.013
Watanabe Y, Gould E, McEwen BS (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588(2):341–345
Wenzel J, Lammert G, Meyer U, Krug M (1991) The influence of long-term potentiation on the spatial relationship between astrocyte processes and potentiated synapses in the dentate gyrus neuropil of rat brain. Brain Res 560(1–2):122–131
Wilhelmsson U, Bushong EA, Price DL, Smarr BL, Phung V, Terada M et al (2006) Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc Natl Acad Sci USA 103(46):17513–17518. https://doi.org/10.1073/pnas.0602841103
Yao X, Hrabetova S, Nicholson C, Manley GT (2008) Aquaporin-4-deficient mice have increased extracellular space without tortuosity change. J Neurosci 28(21):5460–5464. https://doi.org/10.1523/JNEUROSCI.0257-08.2008
Author information
Authors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Bennett, M., Lagopoulos, J. (2018). Synaptic Changes Responsible for Grey Matter Changes in the Brain of Animal Models Following Stress. In: Stress, Trauma and Synaptic Plasticity. Springer, Cham. https://doi.org/10.1007/978-3-319-91116-8_2
Download citation
DOI: https://doi.org/10.1007/978-3-319-91116-8_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-91115-1
Online ISBN: 978-3-319-91116-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)