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Erschienen in: Experimental Brain Research 3/2004

01.10.2004 | Research Article

Effects of somatosensory electrical stimulation on neuronal injury after global hypoxia-ischemia

verfasst von: Manuel M. Buitrago, Andreas R. Luft, Nitish V. Thakor, Mary E. Blue, Daniel F. Hanley

Erschienen in: Experimental Brain Research | Ausgabe 3/2004

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Abstract

Electrical stimulation (ES) is used after cardiac arrest (CA) for diagnostic and therapeutic purposes. The effects of ES on brain damage induced by hypoxic-ischemic brain injury (HI) has not been investigated. Stimulation of afferent pathways by ES may increase neural injury by releasing excitatory neurotransmitters (glutamate) and thereby exacerbating excitotoxicity. To test this hypothesis, ES was applied to the median nerve (2 h) of adult male Wistar rats after 5 min of asphyxic CA and cardiopulmonary resuscitation. Control animals received no ES. Assessment of neuronal damage in five regions of interest was performed in survivors (ES n=15, Control n=10, Sham n=3) after 48 h using H&E, Cresyl-Violet, and TUNEL stains, and Caspase-3 and activated ERK 1/2 immunohistochemistry. Ratios of injured to normal cells were calculated. Most injury was found in hippocampus and cerebellum. ES animals showed significantly lower injury ratios in bilateral hippocampus as compared with controls (F=20.8, p<0.00001). TUNEL staining, caspase-3 and activated ERK 1/2 showed no differences between groups. It is concluded that ES during the acute phase of HI does not amplify neuronal damage at 48 h, but may have a protective effect that requires further investigation.
Literatur
Zurück zum Zitat Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286:1358–1362CrossRefPubMed Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286:1358–1362CrossRefPubMed
Zurück zum Zitat Carter BG, Butt W (2001) Review of the use of somatosensory evoked potentials in the prediction of outcome after severe brain injury. Crit Care Med 29:178–186CrossRefPubMed Carter BG, Butt W (2001) Review of the use of somatosensory evoked potentials in the prediction of outcome after severe brain injury. Crit Care Med 29:178–186CrossRefPubMed
Zurück zum Zitat Choi DW (1988a) Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci 11:465–469PubMed Choi DW (1988a) Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci 11:465–469PubMed
Zurück zum Zitat Choi DW (1988b) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623–634PubMed Choi DW (1988b) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623–634PubMed
Zurück zum Zitat Cooper JB, Jane JA, Alves WM, Cooper EB (1999) Right median nerve electrical stimulation to hasten awakening from coma. Brain Inj 13:261–267CrossRefPubMed Cooper JB, Jane JA, Alves WM, Cooper EB (1999) Right median nerve electrical stimulation to hasten awakening from coma. Brain Inj 13:261–267CrossRefPubMed
Zurück zum Zitat Edgren E, Hedstrand U, Kelsey S, Sutton-Tyrrell K, Safar P (1994) Assessment of neurological prognosis in comatose survivors of cardiac arrest. BRCT I Study Group. Lancet 343:1055–1059CrossRefPubMed Edgren E, Hedstrand U, Kelsey S, Sutton-Tyrrell K, Safar P (1994) Assessment of neurological prognosis in comatose survivors of cardiac arrest. BRCT I Study Group. Lancet 343:1055–1059CrossRefPubMed
Zurück zum Zitat Eke A, Conger KA, Anderson M, Garcia JH (1990) Histologic assessment of neurons in rat models of cerebral ischemia. Stroke 21:299–304PubMed Eke A, Conger KA, Anderson M, Garcia JH (1990) Histologic assessment of neurons in rat models of cerebral ischemia. Stroke 21:299–304PubMed
Zurück zum Zitat Farber JL, Chien KR, Mittnacht S Jr (1981) Myocardial ischemia: the pathogenesis of irreversible cell injury in ischemia. Am J Pathol 102:271–281PubMed Farber JL, Chien KR, Mittnacht S Jr (1981) Myocardial ischemia: the pathogenesis of irreversible cell injury in ischemia. Am J Pathol 102:271–281PubMed
Zurück zum Zitat Garcia JH (1988) Morphology of global cerebral ischemia. Crit Care Med 16:979–987PubMed Garcia JH (1988) Morphology of global cerebral ischemia. Crit Care Med 16:979–987PubMed
Zurück zum Zitat Garcia JH, Lossinsky AS, Kauffman FC, Conger KA (1978) Neuronal ischemic injury: light microscopy, ultrastructure and biochemistry. Acta Neuropathol (Berl) 43:85–95 Garcia JH, Lossinsky AS, Kauffman FC, Conger KA (1978) Neuronal ischemic injury: light microscopy, ultrastructure and biochemistry. Acta Neuropathol (Berl) 43:85–95
Zurück zum Zitat Garcia JH, Liu KF, Ho KL (1995) Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke 26:636–642PubMed Garcia JH, Liu KF, Ho KL (1995) Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke 26:636–642PubMed
Zurück zum Zitat Gavrieli Y, Sherman Y, Ben Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493–501PubMed Gavrieli Y, Sherman Y, Ben Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493–501PubMed
Zurück zum Zitat Geocadin RG, Muthuswamy J, Sherman DL, Thakor NV, Hanley DF (2000) Early electrophysiological and histologic changes after global cerebral ischemia in rats. Mov Disord 15[Suppl 1]: 14–21 Geocadin RG, Muthuswamy J, Sherman DL, Thakor NV, Hanley DF (2000) Early electrophysiological and histologic changes after global cerebral ischemia in rats. Mov Disord 15[Suppl 1]: 14–21
Zurück zum Zitat Gil Z, Amitai Y (1996) Adult thalamocortical transmission involves both NMDA and non-NMDA receptors. J Neurophysiol 76:2547–2554PubMed Gil Z, Amitai Y (1996) Adult thalamocortical transmission involves both NMDA and non-NMDA receptors. J Neurophysiol 76:2547–2554PubMed
Zurück zum Zitat Grant ER, Errico MA, Emanuel SL, Benjamin D, McMillian MK, Wadsworth SA, Zivin RA, Zhong Z (2001) Protection against glutamate toxicity through inhibition of the p44/42 mitogen-activated protein kinase pathway in neuronally differentiated P19 cells. Biochem Pharmacol 62:283–296CrossRefPubMed Grant ER, Errico MA, Emanuel SL, Benjamin D, McMillian MK, Wadsworth SA, Zivin RA, Zhong Z (2001) Protection against glutamate toxicity through inhibition of the p44/42 mitogen-activated protein kinase pathway in neuronally differentiated P19 cells. Biochem Pharmacol 62:283–296CrossRefPubMed
Zurück zum Zitat Guerreiro CA, Ehrenberg BL (1982) Somatosensory evoked response: application in neurology. Arq Neuropsiquiatr 40:29–38PubMed Guerreiro CA, Ehrenberg BL (1982) Somatosensory evoked response: application in neurology. Arq Neuropsiquiatr 40:29–38PubMed
Zurück zum Zitat Hardingham GE, Arnold FJ, Bading H (2001) A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat Neurosci 4:565–566CrossRefPubMed Hardingham GE, Arnold FJ, Bading H (2001) A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat Neurosci 4:565–566CrossRefPubMed
Zurück zum Zitat Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405–414PubMed Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405–414PubMed
Zurück zum Zitat Haupt WF, Birkmann C, Halber M (2000) Serial evoked potentials and outcome in cerebrovascular critical care patients. J Clin Neurophysiol 17:326–330CrossRefPubMed Haupt WF, Birkmann C, Halber M (2000) Serial evoked potentials and outcome in cerebrovascular critical care patients. J Clin Neurophysiol 17:326–330CrossRefPubMed
Zurück zum Zitat Hosobuchi Y, Yingling C (1993) The treatment of prolonged coma with neurostimulation. Adv Neurol 63:247–251PubMed Hosobuchi Y, Yingling C (1993) The treatment of prolonged coma with neurostimulation. Adv Neurol 63:247–251PubMed
Zurück zum Zitat Hu BR, Liu CL, Park DJ (2000) Alteration of MAP kinase pathways after transient forebrain ischemia. J Cereb Blood Flow Metab 20:1089–1095PubMed Hu BR, Liu CL, Park DJ (2000) Alteration of MAP kinase pathways after transient forebrain ischemia. J Cereb Blood Flow Metab 20:1089–1095PubMed
Zurück zum Zitat Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3:661–669PubMed Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3:661–669PubMed
Zurück zum Zitat Irving EA, Barone FC, Reith AD, Hadingham SJ, Parsons AA (2000) Differential activation of MAPK/ERK and p38/SAPK in neurones and glia following focal cerebral ischaemia in the rat. Mol Brain Res 77:65–75PubMed Irving EA, Barone FC, Reith AD, Hadingham SJ, Parsons AA (2000) Differential activation of MAPK/ERK and p38/SAPK in neurones and glia following focal cerebral ischaemia in the rat. Mol Brain Res 77:65–75PubMed
Zurück zum Zitat Jaarsma D, Sebens JB, Korf J (1991) Localization of NMDA and AMPA receptors in rat barrel field. Neurosci Lett 133:233–236CrossRefPubMed Jaarsma D, Sebens JB, Korf J (1991) Localization of NMDA and AMPA receptors in rat barrel field. Neurosci Lett 133:233–236CrossRefPubMed
Zurück zum Zitat Kanno T, Kamel Y, Yokoyama T, Jain VK (1987) Neurostimulation for patients in vegetative status. Pacing Clin Electrophysiol 10:207–208PubMed Kanno T, Kamel Y, Yokoyama T, Jain VK (1987) Neurostimulation for patients in vegetative status. Pacing Clin Electrophysiol 10:207–208PubMed
Zurück zum Zitat Kanno T, Kamel Y, Yokoyama T, Shoda M, Tanji H, Nomura M (1989) Effects of dorsal column spinal cord stimulation (DCS) on reversibility of neuronal function—experience of treatment for vegetative states. Pacing Clin Electrophysiol 12:733–738PubMed Kanno T, Kamel Y, Yokoyama T, Shoda M, Tanji H, Nomura M (1989) Effects of dorsal column spinal cord stimulation (DCS) on reversibility of neuronal function—experience of treatment for vegetative states. Pacing Clin Electrophysiol 12:733–738PubMed
Zurück zum Zitat Katz L, Ebmeyer U, Safar P, Radovsky A, Neumar R (1995) Outcome model of asphyxial cardiac arrest in rats. J Cereb Blood Flow Metab 15:1032–1039PubMed Katz L, Ebmeyer U, Safar P, Radovsky A, Neumar R (1995) Outcome model of asphyxial cardiac arrest in rats. J Cereb Blood Flow Metab 15:1032–1039PubMed
Zurück zum Zitat Kharazia VN, Weinberg RJ (1994) Glutamate in thalamic fibers terminating in layer IV of primary sensory cortex. J Neurosci 14:6021–6032PubMed Kharazia VN, Weinberg RJ (1994) Glutamate in thalamic fibers terminating in layer IV of primary sensory cortex. J Neurosci 14:6021–6032PubMed
Zurück zum Zitat Luft AR, Buitrago MM, Paul JS, Hagan J, Ding MC, Thakor N, Hanley DF (2002) Early restitution of electrocorticogram predicts subsequent behavioral recovery from cardiac arrest. J Clin Neurophysiol (in press) Luft AR, Buitrago MM, Paul JS, Hagan J, Ding MC, Thakor N, Hanley DF (2002) Early restitution of electrocorticogram predicts subsequent behavioral recovery from cardiac arrest. J Clin Neurophysiol (in press)
Zurück zum Zitat Muthuswamy J, Chao J, Sherman D, Thakor NV (1997) Characteristics of thalamic multi-unit activity and EEG during recovery from asphyxia. 19th Ann Internatl Conf of IEEE EMBS, Chicago (Abstract) Muthuswamy J, Chao J, Sherman D, Thakor NV (1997) Characteristics of thalamic multi-unit activity and EEG during recovery from asphyxia. 19th Ann Internatl Conf of IEEE EMBS, Chicago (Abstract)
Zurück zum Zitat Muthuswamy J, Tran P, Rangarajan R, Lenz FA, Hanley DF, Thakor NV (1999) Somatosensory stimulus entrains spindle oscillations in the thalamic VPL nucleus in barbiturate anesthetized rats. Neurosci Lett 262:191–194CrossRefPubMed Muthuswamy J, Tran P, Rangarajan R, Lenz FA, Hanley DF, Thakor NV (1999) Somatosensory stimulus entrains spindle oscillations in the thalamic VPL nucleus in barbiturate anesthetized rats. Neurosci Lett 262:191–194CrossRefPubMed
Zurück zum Zitat Muthuswamy J, Kimura T, Ding MC, Geocadin R, Hanley DF, Thakor NV (2002) Vulnerability of the thalamic somatosensory pathway after prolonged global hypoxic-ischemic injury. Neuroscience 115:917–929CrossRefPubMed Muthuswamy J, Kimura T, Ding MC, Geocadin R, Hanley DF, Thakor NV (2002) Vulnerability of the thalamic somatosensory pathway after prolonged global hypoxic-ischemic injury. Neuroscience 115:917–929CrossRefPubMed
Zurück zum Zitat Nakabayashi M, Kurokawa A, Yamamoto Y (2001) Immediate prediction of recovery of consciousness after cardiac arrest. Intensive Care Med 27:1210–1214CrossRefPubMed Nakabayashi M, Kurokawa A, Yamamoto Y (2001) Immediate prediction of recovery of consciousness after cardiac arrest. Intensive Care Med 27:1210–1214CrossRefPubMed
Zurück zum Zitat Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanai K, Kominami E, Uchiyama Y (1995) Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 15:1001–1011PubMed Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanai K, Kominami E, Uchiyama Y (1995) Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 15:1001–1011PubMed
Zurück zum Zitat Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press
Zurück zum Zitat Plum F (1991) Vulnerability of the brain and heart after cardiac arrest. N Engl J Med 324:1278–1280PubMed Plum F (1991) Vulnerability of the brain and heart after cardiac arrest. N Engl J Med 324:1278–1280PubMed
Zurück zum Zitat Radovsky A, Katz L, Ebmeyer U, Safar P (1997) Ischemic neurons in rat brains after 6, 8, or 10 min of transient hypoxic ischemia. Toxicol Pathol 25:500–505PubMed Radovsky A, Katz L, Ebmeyer U, Safar P (1997) Ischemic neurons in rat brains after 6, 8, or 10 min of transient hypoxic ischemia. Toxicol Pathol 25:500–505PubMed
Zurück zum Zitat Rogove HJ, Safar P, Sutton-Tyrrell K, Abramson NS (1995) Old age does not negate good cerebral outcome after cardiopulmonary resuscitation: analyses from the brain resuscitation clinical trials. The Brain Resuscitation Clinical Trial I and II Study Groups. Crit Care Med 23:18–25CrossRefPubMed Rogove HJ, Safar P, Sutton-Tyrrell K, Abramson NS (1995) Old age does not negate good cerebral outcome after cardiopulmonary resuscitation: analyses from the brain resuscitation clinical trials. The Brain Resuscitation Clinical Trial I and II Study Groups. Crit Care Med 23:18–25CrossRefPubMed
Zurück zum Zitat Rothstein TL (2000) The role of evoked potentials in anoxic-ischemic coma and severe brain trauma. J Clin Neurophysiol 17:486–497CrossRefPubMed Rothstein TL (2000) The role of evoked potentials in anoxic-ischemic coma and severe brain trauma. J Clin Neurophysiol 17:486–497CrossRefPubMed
Zurück zum Zitat Sandroni C, Barelli A, Piazza O, Proietti R, Mastria D, Boninsegna R (1995) What is the best test to predict outcome after prolonged cardiac arrest? Eur J Emerg Med 2:33–37PubMed Sandroni C, Barelli A, Piazza O, Proietti R, Mastria D, Boninsegna R (1995) What is the best test to predict outcome after prolonged cardiac arrest? Eur J Emerg Med 2:33–37PubMed
Zurück zum Zitat Saraste A, Pulkki K (2000) Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 45:528–537PubMed Saraste A, Pulkki K (2000) Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 45:528–537PubMed
Zurück zum Zitat Skaper SD, Facci L, Strijbos PJ (2001) Neuronal protein kinase signaling cascades and excitotoxic cell death. Ann N Y Acad Sci 939:11–22PubMed Skaper SD, Facci L, Strijbos PJ (2001) Neuronal protein kinase signaling cascades and excitotoxic cell death. Ann N Y Acad Sci 939:11–22PubMed
Zurück zum Zitat Sturm V, Kuhner A, Schmitt HP, Assmus H, Stock G (1979) Chronic electrical stimulation of the thalamic unspecific activating system in a patient with coma due to midbrain and upper brain stem infarction. Acta Neurochir (Wien) 47:235–244 Sturm V, Kuhner A, Schmitt HP, Assmus H, Stock G (1979) Chronic electrical stimulation of the thalamic unspecific activating system in a patient with coma due to midbrain and upper brain stem infarction. Acta Neurochir (Wien) 47:235–244
Zurück zum Zitat Sugino T, Nozaki K, Takagi Y, Hattori I, Hashimoto N, Moriguchi T, Nishida E (2000) Activation of mitogen-activated protein kinases after transient forebrain ischemia in gerbil hippocampus. J Neurosci 20:4506–4514PubMed Sugino T, Nozaki K, Takagi Y, Hattori I, Hashimoto N, Moriguchi T, Nishida E (2000) Activation of mitogen-activated protein kinases after transient forebrain ischemia in gerbil hippocampus. J Neurosci 20:4506–4514PubMed
Zurück zum Zitat Sweatt JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1–10CrossRefPubMed Sweatt JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1–10CrossRefPubMed
Zurück zum Zitat Vorob’ev NA, Bakharev BV, Pavlik VD, Zhadin MN (1994) [The phasic relations between the rhythmic activities of the rabbit cortical structures at different frequencies of stimulation of the midbrain reticular formation]. Zh Vyssh Nerv Deiat Im I P Pavlova 44:1038–1045PubMed Vorob’ev NA, Bakharev BV, Pavlik VD, Zhadin MN (1994) [The phasic relations between the rhythmic activities of the rabbit cortical structures at different frequencies of stimulation of the midbrain reticular formation]. Zh Vyssh Nerv Deiat Im I P Pavlova 44:1038–1045PubMed
Zurück zum Zitat Wilson SL, Powell GE, Elliott K, Thwaites H (1991) Sensory stimulation in prolonged coma: four single case studies. Brain Inj 5:393–400PubMed Wilson SL, Powell GE, Elliott K, Thwaites H (1991) Sensory stimulation in prolonged coma: four single case studies. Brain Inj 5:393–400PubMed
Zurück zum Zitat Zandbergen EG, de Haan RJ, Stoutenbeek CP, Koelman JH, Hijdra A (1998) Systematic review of early prediction of poor outcome in anoxic-ischaemic coma. Lancet 352:1808–1812PubMed Zandbergen EG, de Haan RJ, Stoutenbeek CP, Koelman JH, Hijdra A (1998) Systematic review of early prediction of poor outcome in anoxic-ischaemic coma. Lancet 352:1808–1812PubMed
Zurück zum Zitat Zhang J, Benveniste H, Klitzman B, Piantadosi CA (1995) Nitric oxide synthase inhibition and extracellular glutamate concentration after cerebral ischemia/reperfusion. Stroke 26:298–304PubMed Zhang J, Benveniste H, Klitzman B, Piantadosi CA (1995) Nitric oxide synthase inhibition and extracellular glutamate concentration after cerebral ischemia/reperfusion. Stroke 26:298–304PubMed
Metadaten
Titel
Effects of somatosensory electrical stimulation on neuronal injury after global hypoxia-ischemia
verfasst von
Manuel M. Buitrago
Andreas R. Luft
Nitish V. Thakor
Mary E. Blue
Daniel F. Hanley
Publikationsdatum
01.10.2004
Erschienen in
Experimental Brain Research / Ausgabe 3/2004
Print ISSN: 0014-4819
Elektronische ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-004-1906-1

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