Ischemia-induced disturbance of neuronal network function in the rat spinal cord analyzed by voltage-imaging

K. Fukuda, Y. Okada, H. Yoshida, R. Aoyama, Masaya Nakamura, K. Chiba, Y. Toyama

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Using a voltage-imaging technique, we analyzed the acute effect of ischemia, hypoxia and hypoglycemia on the neuronal network function of the rat spinal cord. Ischemic, hypoxic, or hypoglycemic stress was loaded to spinal cord slices with an oxygen- and glucose-free, oxygen-free, or glucose-free mock cerebrospinal fluid, respectively. Depolarizing signals in the dorsal horn, induced by dorsal root stimulation, consisted of fast (pre-synaptic) and slow (post-synaptic) components. The slow component was attenuated much more than the fast component under an ischemic condition (P<0.0002). Post-synaptic neuronal activities in lamina III-IV were suppressed earlier than those in lamina I-II. The nerve fiber was relatively resistant to ischemia. As long as the fast component was preserved in the dorsal horn, the suppression of the fast and slow components was reversible. There was a significant difference (P<0.05) in the recovered slow component sizes between the group in which the fast component was suppressed by more than 20% by ischemia and the group in which the suppression was less than 20%. Further prolonged stress irreversibly eliminated most of the slow component, and attenuated the fast component (to 59±8%) accompanied by cellular damage in histology. Suppression of neural activity by hypoxic or hypoglycemic stress was less prominent than that by ischemia. Prolonged ischemic stress suddenly and irreversibly eliminated depolarizing signals in the ventral horn accompanied by morphological damage of motoneurons. Immunohistochemical staining was negative for apoptosis. We have, for the first time, analyzed the processes of spinal cord disturbance induced by ischemia, hypoxia and hypoglycemia at the neuronal network level by directly observing the regional neuronal network activities within the spinal cord. We conclude that synaptic transmission in the dorsal horn, especially in deep regions, is vulnerable and first affected by these stresses. Severe ischemic stress induces irreversible dysfunction of neurons accompanied by eventual cell death in both dorsal and ventral horns.

Original languageEnglish
Pages (from-to)1453-1465
Number of pages13
JournalNeuroscience
Volume140
Issue number4
DOIs
Publication statusPublished - 2006

Fingerprint

Spinal Cord
Ischemia
Hypoglycemia
Hypoglycemic Agents
Oxygen
Glucose
Negative Staining
Spinal Nerve Roots
Motor Neurons
Horns
Nerve Fibers
Synaptic Transmission
Cerebrospinal Fluid
Spinal Cord Dorsal Horn
Histology
Cell Death
Apoptosis
Neurons
Hypoxia

Keywords

  • hypoglycemia
  • hypoxia
  • membrane potential
  • optical monitoring
  • synaptic transmission
  • voltage-sensitive dye

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Ischemia-induced disturbance of neuronal network function in the rat spinal cord analyzed by voltage-imaging. / Fukuda, K.; Okada, Y.; Yoshida, H.; Aoyama, R.; Nakamura, Masaya; Chiba, K.; Toyama, Y.

In: Neuroscience, Vol. 140, No. 4, 2006, p. 1453-1465.

Research output: Contribution to journalArticle

Fukuda, K. ; Okada, Y. ; Yoshida, H. ; Aoyama, R. ; Nakamura, Masaya ; Chiba, K. ; Toyama, Y. / Ischemia-induced disturbance of neuronal network function in the rat spinal cord analyzed by voltage-imaging. In: Neuroscience. 2006 ; Vol. 140, No. 4. pp. 1453-1465.
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