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2017 | 77 | 1 |

Tytuł artykułu

Effects of epidural compression on stellate neurons and thalamocortical afferent fibers in the rat primary somatosensory cortex

Warianty tytułu

Języki publikacji

EN

Abstrakty

EN
A number of neurological disorders such as epidural hematoma can cause compression of cerebral cortex. We here tested the hypothesis that sustained compression of primary somatosensory cortex may affect stellate neurons and thalamocortical afferent (TCA) fibers. A rat model with barrel cortex subjected to bead epidural compression was used. Golgi‑Cox staining analyses showed the shrinkage of dendritic arbors and the stripping of dendritic spines of stellate neurons for at least 3 months post‑lesion. Anterograde tracing analyses exhibited a progressive decline of TCA fiber density in barrel field for 6 months post‑lesion. Due to the abrupt decrease of TCA fiber density at 3 days after compression, we further used electron microscopy to investigate the ultrastructure of TCA fibers at this time. Some TCA fiber terminal profiles with dissolved or darkened mitochondria and fewer synaptic vesicles were distorted and broken. Furthermore, the disruption of mitochondria and myelin sheath was observed in some myelinated TCA fibers. In addition, expressions of oxidative markers 3‑nitrotyrosine and 4‑hydroxynonenal were elevated in barrel field post‑lesion. Treatment of antioxidant ascorbic acid or apocynin was able to reverse the increase of oxidative stress and the decline of TCA fiber density, rather than the shrinkage of dendrites and the stripping of dendritic spines of stellate neurons post‑lesion. Together, these results indicate that sustained epidural compression of primary somatosensory cortex affects the TCA fibers and the dendrites of stellate neurons for a prolonged period. In addition, oxidative stress is responsible for the reduction of TCA fiber density in barrels rather than the shrinkage of dendrites and the stripping of dendritic spines of stellate neurons.

Słowa kluczowe

Wydawca

-

Rocznik

Tom

77

Numer

1

Opis fizyczny

p.1-17,fig.,ref.

Twórcy

autor
  • Institute of Medical Sciences, Tzu Chi University, Hualien, Taiwan
autor
  • Department of Anatomy, Tzu Chi University, Hualien, Taiwan
  • Institute of Physiological and Anatomical Medicine, Tzu Chi University, Hualien, Taiwan
autor
  • Department of Neurology, Taichung Tzu Chi Hospital, Taichung, Taiwan
autor
  • Institute of Physiological and Anatomical Medicine, Tzu Chi University, Hualien, Taiwan
autor
  • Institute of Medical Sciences, Tzu Chi University, Hualien, Taiwan
  • Department of Anatomy, Tzu Chi University, Hualien, Taiwan
  • Institute of Physiological and Anatomical Medicine, Tzu Chi University, Hualien, Taiwan

Bibliografia

  • Afanas’ev IB (2007) Signaling functions of free radicals superoxide & nitric oxide under physiological & pathological conditions. Mol Biotechnol 37: 2–4.
  • Ansari MA, Roberts KN, Scheff SW (2008) A time course of contusion‑induced oxidative stress and synaptic proteins in cortex in a rat model of TBI. J Neurotrauma 25: 513–526.
  • Awasthi D, Church DF, Torbati D, Carey ME, Pryor WA (1997) Oxidative stress following traumatic brain injury in rats. Surg Neurol 47: 575–581.
  • Ballester‑Rosado CJ, Sun H, Huang JY, Lu HC (2016) mGluR5 exerts cell‑autonomous influences on the functional and anatomical development of layer IV cortical neurons in the mouse primary somatosensory cortex. J Neurosci 36: 8802–8814.
  • Beckman JS, Koppenol WH (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271: C1424–C1437.
  • Blumbergs PC, Scott G, Manavis J, Wainwright H, Simpson DA, McLean AJ (1994) Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet 344: 1055–1056.
  • Buki A, Siman R, Trojanowski JQ, Povlishock JT (1999) The role of calpain‑mediated spectrin proteolysis in traumatically induced axonal injury. J Neuropathol Exp Neurol 58: 365–375.
  • Burnett MG, Detre JA, Greenberg JH (2005) Activation‑flow coupling during graded cerebral ischemia. Brain Res 1047: 112–118.
  • Castejon OJ (1998) Electron microscopic analysis of cortical biopsies in patients with traumatic brain injuries and dysfunction of neurobehavioural system. J Submicrosc Cytol Pathol 30: 145–156.
  • Chen LJ, Wang YJ, Chen JR, Tseng GF (2015) NMDA receptor triggered molecular cascade underlies compression‑induced rapid dendritic spine plasticity in cortical neurons. Exp Neurol 266: 86–98.
  • Chen JR, Wang YJ, Tseng GF (2003) The effect of epidural compression on cerebral cortex: a rat model. J Neurotrauma 20: 767–780.
  • Chen LJ, Wang YJ, Tseng GF (2010a) Compression alters kinase and phosphatase activity and tau and MAP2 phosphorylation transiently while inducing the fast adaptive dendritic remodeling of underlying cortical neurons. J Neurotrauma 27: 1657–1669.
  • Chen JR, Wang TJ, Wang YJ, Tseng GF (2010b) The immediate large‑scale dendritic plasticity of cortical pyramidal neurons subjected to acute epidural compression. Neuroscience 167: 414–427.
  • Conti AC, Raghupathi R, Trojanowski JQ, McIntosh TK (1998) Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post‑traumatic period. J Neurosci 18: 5663–5672.
  • DeAngelis LM (2001) Brain tumors. N Engl J Med 344: 114–123.
  • de la Monte SM, Neely TR, Cannon J, Wands JR (2000) Oxidative stress and hypoxia‑like injury cause Alzheimer‑type molecular abnormalities in central nervous system neurons. Cell Mol Life Sci 57: 1471–1481.
  • Dobkin BH (1991) The rehabilitation of elderly stroke patients. Clin Geriatr Med 7: 507–523.
  • Ferezou I, Haiss F, Gentet LJ, Aronoff R, Weber B, Petersen CC (2007) Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56: 907–923.
  • Furuta T, Deschenes  M, Kaneko T (2011) Anisotropic distribution of thalamocortical boutons in barrels. J Neurosci 31: 6432–6439.
  • Gallace A, Spence C (2009) The cognitive and neural correlates of tactile memory. Psychol Bull 135: 380–406.
  • Gao X, Chen J (2011) Mild traumatic brain injury results in extensive neuronal degeneration in the cerebral cortex. J Neuropathol Exp Neurol 70: 183–191.
  • Grossman KJ, Stein DG (2000) Does endogenous progesterone promote recovery of chronic sensorimotor deficits following contusion to the forelimb representation of the sensorimotor cortex? Behav Brain Res 116: 141–148.
  • Grünewald RA (1993) Ascorbic acid in the brain. Brain Res Brain Res Rev 18: 123–133.
  • Halpain S, Hipolito A, Saffer  L (1998) Regulation of F‑actin stability in dendritic spines by glutamate receptors and calcineurin. J Neurosci 18: 9835–9844.
  • Hayama T, Ogawa H (1997) Regional differences of callosal connections in the granular zones of the primary somatosensory cortex in rats. Brain Res Bull 43: 341–347.
  • Johansson RS, Cole KJ (1992) Sensory‑motor coordination during grasping and manipulative actions. Curr Opin Neurobiol 2: 815–823.
  • Kao C, Forbes JA, Jermakowicz WJ, Sun DA, Davis B, Zhu J, Lagrange AH, Konrad PE (2012) Suppression of thalamocortical oscillations following traumatic brain injury in rats. J Neurosurg 117: 316–323.
  • Kharazia VN, Weinberg RJ (1994) Glutamate in thalamic fibers terminating in layer IV of primary sensory cortex. J Neurosci 14: 6021–6032.
  • Kundrotiene J, Wagner A, Liljequist S (2002) Extradural compression of sensorimotor cortex: a  useful model for studies on ischemic brain damage and neuroprotection. J Neurotrauma 19: 69–84.
  • Kuypers NJ, Hoane MR (2010) Pyridoxine administration improves behavioral and anatomical outcome after unilateral contusion injury in the rat. J Neurotrauma 27: 1275–1282.
  • Lewen A, Hillered  L (1998) Involvement of reactive oxygen species in membrane phospholipid breakdown and energy perturbation after traumatic brain injury in the rat. J Neurotrauma 15: 521–530.
  • Lin JL, Huang YH, Shen YC, Huang HC, Liu PH (2010) Ascorbic acid prevents blood‑brain barrier disruption and sensory deficit caused by sustained compression of primary somatosensory cortex. J Cereb Blood Flow Metab 30: 1121–1136.
  • Marklund N, Clausen F, Lewander T, Hillered  L (2001) Monitoring of reactive oxygen species production after traumatic brain injury in rats with microdialysis and the 4‑hydroxybenzoic acid trapping method. J Neurotrauma 18: 1217–1227.
  • Martinez M, Brezun JM, Xerri C (2011) Sensorimotor experience influences recovery of forelimb abilities but not tissue loss after focal cortical compression in adult rats. PLoS One 6: e16726.
  • Matthews MA, Carey ME, Soblosky JS, Davidson JF, Tabor SL (1998) Focal brain injury and its effects on cerebral mantle, neurons, and fiber tracks. Brain Res 794: 1–18.
  • Mayer SA, Rincon F (2005) Treatment of intracerebral haemorrhage. Lancet Neurol 4: 662–672.
  • Mendez DR, Cherian  L, Moore N, Arora T, Liu PK, Robertson CS (2004) Oxidative DNA lesions in a  rodent model of traumatic brain injury. J Trauma 56: 1235–1240.
  • Moreira T, Cebers G, Salehi M, Wagner A, Liljequist S (2006) Impaired long‑term habituation is dissociated from increased locomotor activity after sensorimotor cortex compression. Behav Brain Res 167: 9–22.
  • Noh KM, Koh JY (2000) Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes. J Neurosci 20: RC111.
  • Paolin A, Nardin  L, Gaetani P, Rodriguez YBR, Pansarasa O, Marzatico F (2002) Oxidative damage after severe head injury and its relationship to neurological outcome. Neurosurgery 51: 949–954.
  • Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Academic Press, San Diego, California, USA.
  • Pettus EH, Povlishock JT (1996) Characterization of a  distinct set of intra‑axonal ultrastructural changes associated with traumatically induced alteration in axolemmal permeability. Brain Res 722: 1–11.
  • Posmantur RM, Kampfl A, Taft WC, Bhattacharjee  M, Dixon CE, Bao J, Hayes RL (1996) Diminished microtubule‑associated protein 2 (MAP2) immunoreactivity following cortical impact brain injury. J Neurotrauma 13: 125–137.
  • Posmantur RM, Newcomb JK, Kampfl A, Hayes RL (2000) Light and confocal microscopic studies of evolutionary changes in neurofilament proteins following cortical impact injury in the rat. Exp Neurol 161: 15–26.
  • Pratico D, Reiss P, Tang LX, Sung S, Rokach J, McIntosh TK (2002) Local and systemic increase in lipid peroxidation after moderate experimental traumatic brain injury. J Neurochem 80: 894–898.
  • Rice ME, Russo‑Menna I (1998) Differential compartmentalization of brain ascorbate and glutathione between neurons and glia. Neuroscience 82: 1213–1223.
  • Rodriguez‑Paez AC, Brunschwig JP, Bramlett HM (2005) Light and electron microscopic assessment of progressive atrophy following moderate traumatic brain injury in the rat. Acta Neuropathol 109: 603–616.
  • Saatman KE, Graham DI, McIntosh TK (1998) The neuronal cytoskeleton is at risk after mild and moderate brain injury. J Neurotrauma 15: 1047–1058.
  • Sanders MJ, Dietrich WD, Green EJ (2001) Behavioral, electrophysiological, and histopathological consequences of mild fluid‑percussion injury in the rat. Brain Res 904: 141–144.
  • Sato M, Chang E, Igarashi T, Noble LJ (2001) Neuronal injury and loss after traumatic brain injury: time course and regional variability. Brain Res 917: 45–54.
  • Serrano F, Kolluri NS, Wientjes FB, Card JP, Klann E (2003) NADPH oxidase immunoreactivity in the mouse brain. Brain Res 988: 193–198.
  • Shimohama S, Tanino H, Kawakami N, Okamura N, Kodama H, Yamaguchi T, Hayakawa T, Nunomura A, Chiba S, Perry G, Smith MA, Fujimoto S (2000) Activation of NADPH oxidase in Alzheimer’s disease brains. Biochem Biophys Res Commun 273: 5–9.
  • Tammariello SP, Quinn MT, Estus S (2000) NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor‑deprived sympathetic neurons. J Neurosci 20: RC53. Turrigiano G (2012) Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb Perspect Biol 4: a005736.
  • Tyurin VA, Tyurina YY, Borisenko GG, Sokolova TV, Ritov VB, Quinn PJ, Rose  M, Kochanek P, Graham SH, Kagan VE (2000) Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates. J Neurochem 75: 2178–2189.
  • Vlachos A, Helias M, Becker D, Diesmann M, Deller T (2013) NMDA‑receptor inhibition increases spine stability of denervated mouse dentate granule cells and accelerates spine density recovery following entorhinal denervation in vitro. Neurobiol Dis 59: 267–276.
  • Watanabe S, Hoffman JR, Craik RL, Hand PJ, Croul SE, Reivich M, Greenberg JH (2001) A new model of localized ischemia in rat somatosensory cortex produced by cortical compression. Stroke 32: 2615–2623.
  • Welker C, Woolsey TA (1974) Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse. J Comp Neurol 158: 437–453.
  • Wilson MA, Johnston MV, Goldstein GW, Blue ME (2000) Neonatal lead exposure impairs development of rodent barrel field cortex. Proc Natl Acad Sci U S A 97: 5540–5545.
  • Winston CN, Chellappa D, Wilkins T, Barton DJ, Washington PM, Loane  DJ, Zapple DN, Burns MP (2013) Controlled cortical impact results in an extensive loss of dendritic spines that is not mediated by injury‑induced amyloid‑beta accumulation. J Neurotrauma 30: 1966–1972.
  • Wu A, Ying Z, Gomez‑Pinilla F (2006) Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress, synaptic plasticity, and cognition. Exp Neurol 197: 309–317.
  • Yang H, Zhang X, Chopp  M, Jiang F, Schallert T (2006) Local fluorouracil chemotherapy interferes with neural and behavioral recovery after brain tumor‑like mass compression. Behav Brain Res 172: 80–89.
  • Zhang D, Dhillon HS, Mattson MP, Yurek DM, Prasad RM (1999) Immunohistochemical detection of the lipid peroxidation product 4‑hydroxynonenal after experimental brain injury in the rat. Neurosci Lett 272: 57–61.
  • Zhang QG, Laird MD, Han D, Nguyen K, Scott E, Dong Y, Dhandapani KM, Brann DW (2012) Critical role of NADPH oxidase in neuronal oxidative damage and microglia activation following traumatic brain injury. PLoS One 7: e34504.
  • Zuo Y, Yang G, Kwon E, Gan WB (2005) Long‑term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436: 261–265.

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Bibliografia

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