Primary sensory and forebrain motor systems in the newborn brain are preferentially damaged by hypoxia-ischemia

Journal of Comparative Neurology

Volumn 377, Issue 2, 1997, Pages 262-285

  Martin, Lee J ^a   Brambrink, Ansgar ^a   Koehler, Raymond C ^a   Traystman, Richard J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

basal ganglia; cytochrome oxidase; neonatal encephalopathy; O2 deprivation; somatosensory system

Indexed keywords

CYTOCHROME C OXIDASE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; CONTROLLED STUDY; HUMAN; HUMAN CELL; MICROPHOTOGRAPHY; NONHUMAN; PERINATAL DEVELOPMENT; PRIORITY JOURNAL; SOMATOSENSORY CORTEX; SWINE; TISSUE DISTRIBUTION;

ANIMALS; ANIMALS, NEWBORN; ASPHYXIA NEONATORUM; BASAL GANGLIA; BRAIN DAMAGE, CHRONIC; BRAIN ISCHEMIA; CARDIOPULMONARY RESUSCITATION; CEREBRAL PALSY; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT COMPLEX IV; EPILEPSY; FETAL HYPOXIA; HEART ARREST; HUMANS; HYPOXIA, BRAIN; INFANT, NEWBORN; MOTOR CORTEX; NERVE TISSUE PROTEINS; SOMATOSENSORY CORTEX; SWINE;

EID: 0031035626     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970113)377:2<262::AID-CNE8>3.0.CO;2-1     Document Type: Article

References (63)

1. Alexander, G.E. and M.D. Crutcher (1990) Functional architecture of basal ganglia circuits: Neural substrates of parallel processing. Trends Neurosci. 13:266-271.
2. Arsenio-Nunes, M.L., K.A. Hossmann, and E. Frakas-Bargeton (1973) Ultrastructural and histochemical investigation of the cerebral cortex of cat during and after complete ischemia. Acta Neuropathol. (Berl). 26:329-344.
3. Auer, R.N. and B.K. Siesjo (1988) Biological differences between ischemia, hypoglycemia, and epilepsy. Ann Neurol. 24:699-707.
4. Balestrino, M. (1995) Pathophysiology of anoxic depolarization: New findings and a working hypothesis. J. Neurosci. Methods 59:99-103.
5. Ballough, G.P.H., L.J. Martin, F.J. Cann, J.S. Graham, C.D. Smith, C.E. Kling, J.S. Forster, S. Phann, and M.G. Filbert (1995) Microtubule-associated protein 2 (MAP-2): a sensitive marker of seizure-related brain damage. J. Neurosci. Meth. 61:23-32.
6. Bevan, M.D., C.M. Francis, and J.P. Bolam (1995) The glutamate-enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: Convergence with GABA-positive terminals. J. Comp. Neurol. 361:491-511.
7. Cavazutti, M. and T.E. Duffy (1982) Regulation of local cerebral blood flow in normal and hypoxic newborn dogs. Ann. Neurol. 11:247-257.
8. Collins, R.C. and J.W. Olney (1982) Focal cortical seizures cause distant thalamic lesions. Science 218:177-179.
9. Craner, S.L. and R.H. Ray (1991) Somatosensory cortex of the neonatal pig: I. Topographic organization of the primary somatosensory cortex (SI). J. Comp. Neurol. 306:24-38.
10. Danbolt, N.C. (1994) The high affinity uptake system for excitatory amino acids in the brain. Prog. Neurobiol. 44:377-396.
11. Duffy, T.E., M. Cavazutti, N.F. Cruz, and L. Sokoloff (1982) Local cerebral glucose metabolism in newborn dogs: Effects of hypoxia and halothane anesthesia. Ann. Neurol. 11:233-246.
12. Fonnum, F., J. Storm-Mathisen, and I. Divac (1981) Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibers in rat brain. Neuroscience 6:863-873.
13. Fujimoto, K. and H. Kita (1993) Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res. 609:185-192.
14. Gonzalez-Lima, F. and M. Garrosa (1991) Quantitative histochemistry of cytochrome oxidase in rat brain. Neurosci. Lett. 123:251-253.
15. Gordon, K.E., J. Simpson, D. Statman, and F.S. Silverstein (1991) Effects of perinatal stroke on striatal amino acid efflux in rat studied with in vivo microdialysis. Stroke 22:928-932.
16. Graham, D.I. (1992) Hypoxia and vascular disorders. In J.H. Adams and L.W. Duchen (eds): Greenfield's Neuropathology. New York: Oxford University Press, pp. 153-268.
17. 2 deprivation in the central nervous system: On mechanisms of neuronal response, differential sensitivity and injury. Prog. Neurobiol. 40:277-318.
18. Hagberg, H., P. Anderssen, I. Kjellmer, K. Thiringer, and M. Thordstein (1987) Extracellular overflow of glutamate, aspartate, GABA and taurine in the cortex and basal ganglia of fetal lambs during hypoxia-ischemia. Neurosci. Lett. 78:311-317.
19. Hevner, R.F., S. Liu, and M.T.T. Wong-Riley (1995) A metabolic map of cytochrome oxidase in the rat brain: Histochemical, densitometric and biochemical studies. Neuroscience 65:313-342.
20. Holm, I.E., and F.A. Geneser (1991) Histochemical demonstration of zinc in the hippocampal region of the domestic pig: II. Subiculum and hippocampus. J. Comp. Neurol. 305:71-82.
21. Huntley, G.W. and E.G. Jones (1991) The emergence of architectonic field structure and areal borders in developing monkey sensorimotor cortex. Neuroscience 44:287-310.
22. Ikonomidou, C., M.T. Price, J.L. Mosinger, G. Frierdich, J. Labruyere, K.S. Salles, and J.W. Olney (1989) Hypobaric-ischemic conditions produce glutamate-like cytopathology in infant rat brain. J. Neurosci. 9:1693-1700.
23. Jones, E.G., J.D. Coulter, H. Burton, and R. Porter (1977) Cells of origin and terminal distribution of corticostriatal fibers arising in the sensory-motor cortex of monkeys. J. Comp. Neurol. 173:53-80.
24. Jones, E.G., S.H.C. Hendry, and C. Brandon (1986) Cytochrome oxidase staining reveals functional organization of monkey somatosensory thalamus. Exp. Brain Res. 62:438-442.
25. Jorgensen, M.B., D.C. Wright, and N.H. Diemer (1990) Postischemic glucose metabolism is modified in the hippocampal CA1 region depleted of excitatory input or pyramidal cells. J. Cereb. Blood Flow and Metab. 10:243-251.
26. Kaas, J.H., M.M. Merzenich, and H.P. Killackey (1983) The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. Ann. Rev. Neurosci. 6:325-356.
27. Kirino, T. (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 239:57-69.
28. Kolb, B. and I.Q. Whishaw (1989) Plasticity in the neocortex: Mechanisms underlying recovery from early brain damage. Prog. Neurobiol. 32:235-276.
29. Kuban, K.C.K. and A. Leviton (1994) Cerebral palsy. N. Engl. J. Med. 330:188-195.
30. LeBlanc, M.H., V. Vig, B. Smith, C.C. Parker, O.B. Evans, and E.E. Smith (1991) MK-801 does not protect against hypoxic-ischemic brain injury in piglets. Stroke 22:1270-1275.
31. LeBlanc, M.H., X.Q. Li, M. Huang, D.M. Patel, and E.E. Smith (1995) AMPA antagonist LY293558 does not affect the severity of hypoxic-ischemic injury in newborn pigs. Stroke 26:1908-1915.
32. Low, J.A., D.M. Robertson, and L.L. Simpson (1989) Temporal relationships of neuropathologic conditions caused by perinatal asphyxia. Am. J. Obstet. Gynecol. 160:608-614.
33. Martin, L.J., J.A. Doebler, T-M. Shih, and A. Anthony (1985) Protective effect of diazepam pretreatment on soman-induced brain lesion formation. Brain Res. 325:287-289.
34. Martin, L.J., D.W. Spicer, M.H. Lewis, J.P. Gluck, and L.C. Cork (1991) Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: I. Subcortical regions. J. Neurosci. 11:3344-3358.
35. Martin, L.J., C.D. Blackstone, R.L. Huganir, and D.L. Price (1993a) The striatal mosaic in primates: striosomes and matrix are differentially enriched in ionotropic glutamate receptor subunits. J. Neurosci. 13:782-792.
36. Martin, L.J., C.D. Blackstone, A.I. Levey, R.L. Huganir, and D.L. Price (1993b) AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53:327-358.
37. Martin, L.J., A. Brambrink, C. Portera-Cailliau, R.C. Koehler, J.D. Rothstein, and R.J. Traystman (1996) Cerebral hypoxia-ischemia in newborns results in rapid death of astrocytes in striatum: a mechanism for ischemic neurodegeneration. Soc. Neurosci. Abstr. 22:1423.
38. Mujsce, D.J., J. Towfighi, J.Y. Yager, and R.C. Vannucci (1993) Neuropathologic aspects of hypothermic circulatory arrest in newborn dogs. Acta Neuropathol. 85:190-198.
39. Myers, R.E. (1972) Two patterns of perinatal brain damage and their conditions of occurrence. Am. J. Obstet. Gynecol. 112:246-276.
40. Myers, R.E. (1977) Experimental models of perinatal brain damage: Relevance to human pathology. In L. Gluck (ed): Intrauterine Asphyxia and the Developing Fetal Brain. Chicago: Year Book Medical Publishers, pp. 37-97.
41. Nevander, G., M. Ingyar, R. Auer, and B.K. Siesjo (1985) Status epilepticus in well-oxygenated rats causes neuronal necrosis. Ann. Neurol. 18:281-290.
42. Olney, J.W., L.G. Sharpe, and R.D. Feigin (1972) Glutamate-induced brain damage in infant primates. J. Neuropathol. Exp. Neurol. 31:464-488.
43. Petito, C.K., E. Feldmann, W.A. Pulsinelli, and F. Plum (1987) Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 37:1281-1286.
44. Ranck, J.B. and W.F. Windle (1959) Brain damage in the monkey, Macaca mulatta, by asphyxia neonatorum. Exp. Neurol. 1:130-154.
45. Razdan, B., P.J. Marro, O. Tammela, R. Goel, O.P. Mishra, and M. Delivoria-Papadopoulos (1993) Selective sensitivity of synaptosomal membrane function to cerebral cortical hypoxia in newborn piglets. Brain Res. 600:308-314.
46. Rorke, L.B. (1992) Perinatal brain damage. In J.H. Adams and L.W. Duchen (eds): Greenfield's Neuropathology. New York: Oxford University Press, pp. 639-708.
47. Rosene, D.L. and G.W. Van Hoesen (1987) The hippocampal formation of the primate brain: A review of some comparative aspects of cytoarchitecture and connections. In E.G. Jones and A. Peters (eds): Cerebral Cortex, Vol. 6. New York: Plenum Press, pp. 345-456.
48. Rothman, S.M. (1984) Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death. J. Neurosci. 4:1884-1891.
49. Rothstein, J.D., L.J. Martin, A.I. Levey, M. Dykes-Hoberg, L. Jin, D. Wu, N. Nash, and R.W. Kuncl (1994) Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
50. Salt, T.E. and P.L. Herrling (1991) Excitatory amino acid transmitter function in mammalian central pathways. In H. Wheal and A. Thomson (eds): Excitatory Amino Acids and Synaptic Transmission. New York: Academic Press, pp. 155-170.
51. Schneider, H., L. Ballowitz, H. Schachinger, F. Hanefeld, and J.U. Droszus (1975) Anoxic encephalopathy with predominant involvement of basal ganglia, brain stem. and spinal cord in the perinatal period. Report on seven newborns. Acta Neuropathol. (Berl). 32:287-298.
52. Schwartz, P.H., W.F. Massarweh, H.V. Vinters, C.G. Wasterlain (1992) A rat model of severe neonatal hypoxic-ischemic brain injury. Stroke 23:539-546.
53. 3H-glutamate uptake into synaptosomes. J. Neurochem. 47:1615-1619.
54. Solnitzky, O. (1938) The thalamic nuclei of Sus scrofa. J. Comp. Neurol. 69:121-169.
55. Tanaka, T., S. Tanaka, T. Fujita, K. Takano, H. Fukuda, K. Sako, and Y. Yonemasu (1992) Experimental complex partial seizures induced by microinjection of kainic acid into limbic structures. Prog. Neurobiol. 38:317-334.
56. Urban, L., K.H. Neill, B.J. Crain, J.V. Nadler, and G.G. Somjen (1989) Postischemic synaptic physiology in area CA1 of the gerbil hippocampus studied in vitro. J. Neurosci. 9:3966-3975.
57. Volpe, J.J. (1987) Neurology of the Newborn. Philadelphia: Saunders.
58. 14C-2-deoxyglucose uptake and fos immunocytochemistry. J. Neurosci. 13:4787-4809.
59. Wong-Riley, M.T.T. (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 171:11-28.
60. Wong-Riley, M.T.T. (1989) Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends Neurosci. 12:94-101.
61. Woolsey, C.N. and D. Fairman (1946) Contralateral, ipsilateral, and bilateral representation of cutaneous receptors in somatic areas I and II of the cerebral cortex of pig, sheep, and other mammals. Surgery 19:684-702.
62. Yamamoto, T. and A. Hirano (1986) A comparative study of modified Bielschowsky, Bodian, and thioflavin S stains on Alzheimer's neurofibrillary tangles. Neuropathol. Appl. Neurobiol. 12:3-9.
63. Young, R.S.K., R.R. Fripp, S.K. Yagel, J.C. Werner, G. McGrath, and H.G. Schuler (1985) Cardiac dysfunction during status epilepticus in the neonatal pig. Ann. Neurol. 18:291-297.