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The Journal of Neurophysiology Vol. 83 No. 2 February 2000, pp. 1031-1038
Copyright ©2000 by the American Physiological Society
Departments of 1Physiology and
2Pediatrics
Constance Kaufman Research
Laboratory, and 3Neuroscience Program, Tulane
University School of Medicine, New Orleans, Louisiana 70112
Kreisman, Norman R.,
Soheil Soliman, and
David Gozal.
Regional Differences in Hypoxic Depolarization and Swelling in
Hippocampal Slices. J. Neurophysiol. 83: 1031-1038, 2000. Pyramidal neurons in the CA1 region of the
hippocampus are highly vulnerable to damage from hypoxia-ischemia,
whereas neurons in the CA3 region and the dentate gyrus are more
resistant. A similar pattern of vulnerability to loss of synaptic and
membrane function occurs in the in vitro hippocampal slice preparation, suggesting that intrinsic factors are important in acute neuronal damage. Simultaneous recordings of DC potential and imaging of changes
in light transmittance were made in slices from the middle one-third of
the hippocampus to characterize the initiation and spread of
depolarization and swelling during hypoxia-aglycemia. Hypoxic
depolarization (HD) and associated optical changes were initiated
simultaneously in the stratum oriens of the CA1 region and thereafter
spread to the stratum radiatum of CA1 and later to the upper (inner)
blade of the dentate gyrus. A decrease in light transmittance was
associated consistently with depolarization in all regions
(n = 22 slices). Investigation of the sequence of
activation in intact slices showed that activation of the dentate gyrus
arose independently of activation of the CA1 region. This was confirmed
by recordings made from minislices in which CA1, CA3, and dentate
regions were physically separated. HD and optical changes were never
observed in the CA3 region, despite exposure to 40-60 min of combined
hypoxia and aglycemia. In contrast, exposure to hypoxia after
pretreatment of slices with altered tonicity or ion composition, which
triggered episodes of spreading depolarization (SD), provoked
depolarization and optical changes simultaneously in both CA1 and CA3
regions. Similarly, pretreatment with agents that cause severe
metabolic impairment, such as dinitrophenol (DNP), also rendered the
CA3 region vulnerable to subsequent hypoxia. This suggests that the CA3
region in hippocampal slices is normally resistant to HD and only
becomes vulnerable after severe impairment of metabolic capacity. The
similar order of vulnerability of in vitro and in vivo hippocampus to
hypoxia-aglycemia supports the use of the hippocampal slice preparation
to investigate early changes potentially contributing to
hypoxic-ischemic injury.
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