Thalamocortical dysfunction and thalamic injury after asphyxial cardiac arrest in developing rats

Journal of Neuroscience

Volumn 32, Issue 14, 2012, Pages 4972-4981

  Shoykhet, Michael ^a,b,c,d   Simons, Daniel J ^a   Alexander, Henry ^b   Hosler, Christina ^b   Kochanek, Patrick M ^a,b,c   Clark, Robert S B ^a,b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE DECARBOXYLASE 65;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPHYXIA; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; FEMALE; HEART ARREST; HISTOLOGY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOHISTOCHEMISTRY; LATENT PERIOD; MALE; MICROGLIA; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; RESUSCITATION; SENSORY STIMULATION; SOMATOSENSORY SYSTEM; THALAMOCORTICAL TRACT; THALAMUS RETICULAR NUCLEUS; VIBRISSA;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; ASPHYXIA; HEART ARREST; MALE; NEURAL PATHWAYS; NEURITES; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX; THALAMUS; VIBRISSAE;

EID: 84859360974     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5597-11.2012     Document Type: Article

References (74)

1. Arbelaez A, Castillo M, Mukherji SK (1999) Diffusion-weighted MR imaging of global cerebral anoxia. AJNR Am J Neuroradiol 20:999-1007
2. Barbaresi P, Spreafico R, Frassoni C, Rustioni A (1986) GABAergic neurons are present in the dorsal column nuclei but not in the ventroposterior complex of rats. Brain Res 382:305-326
3. Bianchi MT, Sims JR (2008) Restricted diffusion in the splenium of the corpus callosum after cardiac arrest. Open Neuroimag J 2:1-4
4. Böttiger BW, Schmitz B, Wiessner C, Vogel P, Hossmann KA (1998) Neuronal stress response and neuronal cell damage after cardiocirculatory arrest in rats. J Cereb Blood Flow Metab 18:1077-1087
5. Carvell GE, Simons DJ (1996) Abnormal tactile experience early in life disrupts active touch. J Neurosci 16:2750-2757
6. Centers for Disease Control and Prevention (2002) State-specific mortality from sudden cardiac death-United States, 1999. MMWR Morb Mortal Wkly Rep 51:123-126
7. Choi SP, Park KN, Park HK, Kim JY, Youn CS, Ahn KJ, Yim HW (2010) Diffusion-weighted magnetic resonance imaging for predicting the clinical outcome of comatose survivors after cardiac arrest: a cohort study. Crit Care 14:R17
8. Crick F (1984) Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci U S A 81:4586-4590
9. Cummings JL, Tomiyasu U, Read S, Benson DF (1984) Amnesia with hippocampal lesions after cardiopulmonary arrest. Neurology 34:679-681
10. De Olmos JS, Ingram WR (1971) An improved cupric-silver method for impregnation of axonal and terminal degeneration. Brain Res 33:523-529
11. Desai NS, Cudmore RH, Nelson SB, Turrigiano GG (2002) Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci 5:783-789
12. Deschênes M, Timofeeva E, Lavalee P (2003) The relay of high-frequency sensory signals in the whisker-to-barreloid pathway. J Neurosci 23:6778-6787
13. Ergenzinger ER, Glasier MM, Hahm JO, Pons TP (1998) Cortically induced thalamic plasticity in the primate somatosensory system. Nat Neurosci 1:226-229
14. Failor S, Nguyen V, Darcy DP, Cang J, Wendland MF, Stryker MP, McQuillen PS (2010) Neonatal cerebral hypoxia-ischemia impairs plasticity in rat visual cortex. J Neurosci 30:81-92
15. Fink EL, Alexander H, Marco CD, Dixon CE, Kochanek PM, Jenkins LW, Lai Y, Donovan HA, Hickey RW, Clark RS (2004) Experimental model of pediatric asphyxial cardiopulmonary arrest in rats. Pediatr Crit Care Med 5:139-144
16. Fisher LD, van Belle G (1993) Biostatistics: a methodology for the health sciences. New York: Wiley
17. Fujioka M, Okuchi K, Sakaki T, Hiramatsu K, Miyamoto S, Iwasaki S (1994) Specific changes in human brain following reperfusion after cardiac arrest. Stroke 25:2091-2095
18. Garman RH, Jenkins LW, Switzer RC 3rd, Bauman RA, Tong LC, Swauger PV, Parks SA, Ritzel DV, Dixon CE, Clark RS, Bayir H, Kagan V, Jackson EK, Kochanek PM (2011) Blast exposure in rats with body shielding is characterized primarily by diffuse axonal injury. J Neurotrauma 28: 947-959
19. 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
20. Gladstone DJ, Black SE, Hakim AM (2002) Toward wisdom from failure: lessons from neuroprotective stroke trials and new therapeutic directions. Stroke 33:2123-2136
21. Gofton TE, Chouinard PA, Young GB, Bihari F, Nicolle MW, Lee DH, Sharpe MD, Yen YF, Takahashi AM, Mirsattari SM (2009) Functional MRI study of the primary somatosensory cortex in comatose survivors of cardiac arrest. Exp Neurol 217:320-327
22. Graham DI (1977) Pathology of hypoxic brain damage in man. J Clin Pathol Suppl (R Coll Pathol) 11:170-180
23. Graves JR, Herlitz J, Bång A, Axelsson A, Ekström L, Holmberg M, Lindqvist J, Sunnerhagen K, Holmberg S (1997) Survivors of out of hospital cardiac arrest: their prognosis, longevity and functional status. Resuscitation 35:117-121
24. Greer D, Scripko P, Bartscher J, Sims J, Camargo E, Singhal A, Furie K (2011a) Serial MRI changes in comatose cardiac arrest patients. Neurocrit Care 14:61-67
25. Greer JE, McGinn MJ, Povlishock JT (2011b) Diffuse traumatic axonal injury in the mouse induces atrophy, c-Jun activation, and axonal outgrowth in the axotomized neuronal population. J Neurosci 31:5089-5105
26. Harris RM, Hendrickson AE (1987) Local circuit neurons in the rat ventrobasal thalamus-a GABA immunocytochemical study. Neuroscience 21:229-236
27. Hartings JA, Simons DJ (2000) Inhibition suppresses transmission of tonic vibrissa-evoked activity in the rat ventrobasal thalamus. J Neurosci 20: RC100
28. Hartings JA, Temereanca S, Simons DJ (2003) State-dependent processing of sensory stimuli by thalamic reticular neurons. J Neurosci 23:5264-5271
29. Hattox AM, Nelson SB (2007) Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J Neurophysiol 98:3330-3340
30. Hausmann R, Seidl S, Betz P (2007) Hypoxic changes in Purkinje cells of the human cerebellum. Int J Legal Med 121:175-183
31. Horn M, Schlote W (1992) Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol 85:79-87
32. Hossmann KA, Oschlies U, Schwindt W, Krep H (2001) Electron microscopic investigation of rat brain after brief cardiac arrest. Acta Neuropathol 101:101-113
33. Hyde TM, Lipska BK, Ali T, Mathew SV, Law AJ, Metitiri OE, Straub RE, Ye T, Colantuoni C, Herman MM, Bigelow LB, Weinberger DR, Kleinman JE (2011) Expression of GABA signaling molecules KCC2, NKCC1, and GAD1 in cortical development and schizophrenia. J Neurosci 31:11088-11095
34. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S (1996) A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys ResCommun 224:855-862
35. Jones EG (2002) Thalamic circuitry and thalamocortical synchrony. Philos Trans R Soc Lond B Biol Sci 357:1659-1673
36. Khot S, Tirschwell DL (2006) Long-term neurological complications after hypoxic-ischemic encephalopathy. Semin Neurol 26:422-431
37. Kumar K, White BC, Krause GS, Indrieri RJ, Evans AT, Hoehner TJ, Garritano AM, Koestner A (1988) A quantitative morphological assessment of the effect of lidoflazine and deferoxamine therapy on global brain ischaemia. Neurol Res 10:136-140
38. Kwegyir-Afful EE, Bruno RM, Simons DJ, Keller A (2005) The role of thalamic inputs in surround receptive fields of barrel neurons. J Neurosci 25:5926-5934
39. Land PW, Simons DJ (1985) Cytochrome oxidase staining in the rat SmI barrel cortex. J Comp Neurol 238:225-235
40. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157
41. Manole MD, Foley LM, Hitchens TK, Kochanek PM, Hickey RW, Bayir H, Alexander H, Ho C, Clark RS (2009) Magnetic resonance imaging assessment of regional cerebral blood flow after asphyxial cardiac arrest in immature rats. J Cereb Blood Flow Metab 29:197-205
42. Maryniak A, Bielawska A, Walczak F, Szumowski, Bieganowska K, Rekawek J, Paszke M, Szymaniak E, Knecht M (2008) Long-term cognitive outcome in teenage survivors of arrhythmic cardiac arrest. Resuscitation 77:46-50
43. Mateen FJ, Josephs KA, Trenerry MR, Felmlee-Devine MD, Weaver AL, Carone M, White RD (2011) Long-term cognitive outcomes following out-of-hospital cardiac arrest: a population-based study. Neurology 77:1438-1445
44. McAlonan K, Cavanaugh J, Wurtz RH (2008) Guarding the gateway to cortex with attention in visual thalamus. Nature 456:391-394
45. McCormick DA, Bal T (1997) Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci 20:185-215
46. Molnár Z, Cheung AF (2006) Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci Res 55:105-115
47. Myers RE, Yamaguchi S (1977) Nervous system effects of cardiac arrest in monkeys. Preservation of vision. Arch Neurol 34:65-74
48. Ng T, Graham DI, Adams JH, Ford I (1989) Changes in the hippocampus and the cerebellum resulting from hypoxic insults: frequency and distribution. Acta Neuropathol 78:438-443
49. Nichol G, Thomas E, Callaway CW, Hedges J, Powell JL, Aufderheide TP, Rea T, Lowe R, Brown T, Dreyer J, Davis D, Idris A, Stiell I (2008) Regional variation in out-of-hospital cardiac arrest incidence and outcome. JAMA 300:1423-1431
50. Oda Y, Gao G, Wei EP, Povlishock JT (2011) Combinational therapy using hypothermia and the immunophilin ligand FK506 to target altered pial arteriolar reactivity, axonal damage, and blood-brain barrier dysfunction after traumatic brain injury in rat. J Cereb Blood Flow Metab 31:1143-1154
51. Peskine A, Rosso C, Picq C, Caron E, Pradat-Diehl P (2010) Neurological sequelae after cerebral anoxia. Brain Inj 24:755-761
52. Pollock JM, Whitlow CT, Deibler AR, Tan H, Burdette JH, Kraft RA, Maldjian JA (2008) Anoxic injury-associated cerebral hyperperfusion identified with arterial spin-labeled MR imaging. AJNR Am J Neuroradiol 29:1302-1307
53. Pulsinelli WA, Brierley JB (1979) Anew model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10:267-272
54. Radovsky A, Safar P, Sterz F, Leonov Y, Reich H, Kuboyama K (1995) Regional prevalence and distribution of ischemic neurons in dog brains 96 hours after cardiac arrest of 0 to 20 minutes. Stroke 26:2127-2133, discussion 2133-2134
55. Radovsky A, Katz L, Ebmeyer U, Safar P (1997) Ischemic neurons in rat brains after 6, 8, or 10 minutes of transient hypoxic ischemia. Toxicol Pathol 25:500-505
56. Rice JE 3rd, Vannucci RC, Brierley JB (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 9:131-141
57. Rivera C, Voipio J, Kaila K (2005) Two developmental switches in GABAergic signalling: the K_-Cl-cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562:27-36
58. Schmued LC, Albertson C, Slikker W Jr (1997) Fluoro-Jade: a novel fluoro-chrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 751:37-46
59. Sharma HS, Miclescu A, Wiklund L (2011) Cardiac arrest-induced regional blood-brain barrier breakdown, edema formation and brain pathology: a light and electron microscopic study on a new model for neurodegeneration and neuroprotection in porcine brain. J Neural Transm 118:87-114
60. Shoykhet M, Simons DJ (2008) Development of thalamocortical response transformations in the rat whisker-barrel system. J Neurophysiol 99:356-366
61. Shoykhet M, Shetty P, Minnery BS, Simons DJ (2003) Protracted development of responses to whisker deflection in rat trigeminal ganglion neurons. J Neurophysiol 90:1432-1437
62. Shoykhet M, Land PW, Simons DJ (2005) Whisker trimming begun at birth or on postnatal day 12 affects excitatory and inhibitory receptive fields of layer IV barrel neurons. J Neurophysiol 94:3987-3995
63. Simons DJ (1983) Multi-whisker stimulation and its effects on vibrissa units in rat SmI barrel cortex. Brain Res 276:178-182
64. Simons DJ, Carvell GE (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61:311-330
65. Simons DJ, Land PW (1987) Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326:694-697
66. Simons DJ, Carvell GE, Hershey AE, Bryant DP (1992) Responses of barrel cortex neurons in awake rats and effects of urethane anesthesia. Exp Brain Res 91:259-272
67. Stern EA, Maravall M, Svoboda K (2001) Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron 31:305-315
68. Switzer RC 3rd (2000) Application of silver degeneration stains for neurotoxicity testing. Toxicol Pathol 28:70-83
69. Venkatesan A, Frucht S (2006) Movement disorders after resuscitation from cardiac arrest. Neurol Clin 24:123-132
70. Volpe BT, Hirst W (1983) The characterization of an amnesic syndrome following hypoxic ischemic injury. Arch Neurol 40:436-440
71. Volpe BT, Holtzman JD, Hirst W (1986) Further characterization of patients with amnesia after cardiac arrest: preserved recognition memory. Neurology 36:408-411
72. Welker WI (1964) Analysis of sniffing in the albino rat. Behaviour 22:223-244
73. Wintermark M, Lepori D, Cotting J, Roulet E, van Melle G, Meuli R, Maeder P, Regli L, Verdun FR, Deonna T, Schnyder P, Gudinchet F (2004) Brain perfusion in children: evolution with age assessed by quantitative perfusion computed tomography. Pediatrics 113:1642-1652
74. Wong-Riley MT, Merzenich MM, Leake PA (1978) Changes in endogenous enzymatic reactivity to DAB induced by neuronal inactivity. Brain Res 141:185-192.