Electrophysiological changes of CA1 pyramidal neurons following transient forebrain ischemia: An in vivo intracellular recording and staining study

Z. C. Xu, W. A. Pulsinelli

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Abstract

1. Electrophysiological changes of CA1 pyramidal neurons in rat hippocampus were studied before, during 5 min forebrain ischemia, and after reperfusion using in vivo intracellular recording and staining techniques. 2. Membrane input resistance of CA1 neurons decreased from 25.98 ± 7.24 MΩ (mean ± SD, n = 42) before ischemia to 16.33 ± 6.50 MΩ shortly after the onset of ischemia (n = 6, P <0.01). The input resistance fell to zero during ischemic depolarization and quickly returned to 24.42 ± 10.36 MΩ (n = 11) within 2 h after reperfusion. 3. The time constant of CA1 neurons decreased from 11.49 ± 5.45 ms (n = 36) to 3.09 ± 1.66 ms (n = 6, P <0.01) during ischemia. The time constant remained significantly less than preischemic levels within 2 h after reperfusion (5.40 ± 2.60 ms, n = 13, P <0.01) and gradually returned to preischemic levels 4-5 h after reperfusion. 4. The spike height decreased from 91 ± 10.35 mV (n = 45) before ischemia to 82 ± 8.00 mV (n = 9, P <0.05) within 2 h after reperfusion and fully returned to preischemic level 2-5 h after reperfusion. The spike width increased from 1.14 ± 0.22 ms (n = 45) before ischemia to 1.36 ± 0.22 ms (n = 9, P <0.05) within 2 h after reperfusion and remained at this level 4-5 h after reperfusion. 5. The spike threshold significantly increased from -54 ± 3.93 mV (n = 45) before ischemia to 49 ± 5.04 mV (n = 8, P <0.01) within 2 h after reperfusion. The rheobase increased accordingly from 0.34 ± 0.16 nA (n = 41) to 0.73 ± 0.26 nA (n = 6, P <0.01). The spike threshold returned to control levels 4-5 h after reperfusion, while the rheobase was still significantly higher than control levels (0.50 ± 0.21 nA, n = 16, P <0.01). 6. The frequency of repetitive firing evoked by depolarizing current pulses was suppressed within 2 h after reperfusion (n = 6, P <0.01). The spike frequency increased slightly 2-5 h after reperfusion but was still significantly below the control levels (n = 12, P <0.01). 7. Spontaneous synaptic activities ceased during ischemia and remained depressed shortly after reperfusion. Spontaneous firing rate was 0.47 ± 0.81 spikes/s (n = 34) before ischemia. No spontaneous firing was detected within 2 h after reperfusion, and the firing rate gradually returned to preischemic levels 2- 5 h after reperfusion (0.28 ± 0.96 spikes/s, n = 15). Neuronal hyperactivity as indicated by an increased spontaneous firing rate was not observed up to 7 h after reperfusion. 8. Stimulation of the contralateral commissural pathway elicited excitatory postsynaptic potentials (EPSPs) minutes after reperfusion, whereas inhibitory postsynaptic potentials (IPSPs) did not appear until °1 h after reperfusion. Within 2 h after reperfusion, the amplitudes of EPSPs slightly increased compared with those before ischemia, and the duration of EPSPs significantly increased from 18.00 ± 3.08 ms (n = 5) before ischemia to 26.83 ± 4.26 ms (n = 6, P <0.01). The amplitude and duration of EPSPs returned to preischemic levels 4-5 h after reperfusion. 9. Results from the present study indicate that the input resistance and time constant of CA1 pyramidal neurons decrease during cerebral ischemia. After 5 min of forebrain ischemia, the spontaneous neuronal activities, evoked synaptic potentials and excitability of CA1 neurons are transiently suppressed after reperfusion. No hyperactivity was observed up to 7 h after reperfusion.

Original languageEnglish (US)
Pages (from-to)1689-1697
Number of pages9
JournalJournal of Neurophysiology
Volume76
Issue number3
StatePublished - Sep 1996
Externally publishedYes

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Pyramidal Cells
Prosencephalon
Reperfusion
Ischemia
Staining and Labeling
Excitatory Postsynaptic Potentials
Neurons

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Electrophysiological changes of CA1 pyramidal neurons following transient forebrain ischemia : An in vivo intracellular recording and staining study. / Xu, Z. C.; Pulsinelli, W. A.

In: Journal of Neurophysiology, Vol. 76, No. 3, 09.1996, p. 1689-1697.

Research output: Contribution to journalArticle

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abstract = "1. Electrophysiological changes of CA1 pyramidal neurons in rat hippocampus were studied before, during 5 min forebrain ischemia, and after reperfusion using in vivo intracellular recording and staining techniques. 2. Membrane input resistance of CA1 neurons decreased from 25.98 ± 7.24 MΩ (mean ± SD, n = 42) before ischemia to 16.33 ± 6.50 MΩ shortly after the onset of ischemia (n = 6, P <0.01). The input resistance fell to zero during ischemic depolarization and quickly returned to 24.42 ± 10.36 MΩ (n = 11) within 2 h after reperfusion. 3. The time constant of CA1 neurons decreased from 11.49 ± 5.45 ms (n = 36) to 3.09 ± 1.66 ms (n = 6, P <0.01) during ischemia. The time constant remained significantly less than preischemic levels within 2 h after reperfusion (5.40 ± 2.60 ms, n = 13, P <0.01) and gradually returned to preischemic levels 4-5 h after reperfusion. 4. The spike height decreased from 91 ± 10.35 mV (n = 45) before ischemia to 82 ± 8.00 mV (n = 9, P <0.05) within 2 h after reperfusion and fully returned to preischemic level 2-5 h after reperfusion. The spike width increased from 1.14 ± 0.22 ms (n = 45) before ischemia to 1.36 ± 0.22 ms (n = 9, P <0.05) within 2 h after reperfusion and remained at this level 4-5 h after reperfusion. 5. The spike threshold significantly increased from -54 ± 3.93 mV (n = 45) before ischemia to 49 ± 5.04 mV (n = 8, P <0.01) within 2 h after reperfusion. The rheobase increased accordingly from 0.34 ± 0.16 nA (n = 41) to 0.73 ± 0.26 nA (n = 6, P <0.01). The spike threshold returned to control levels 4-5 h after reperfusion, while the rheobase was still significantly higher than control levels (0.50 ± 0.21 nA, n = 16, P <0.01). 6. The frequency of repetitive firing evoked by depolarizing current pulses was suppressed within 2 h after reperfusion (n = 6, P <0.01). The spike frequency increased slightly 2-5 h after reperfusion but was still significantly below the control levels (n = 12, P <0.01). 7. Spontaneous synaptic activities ceased during ischemia and remained depressed shortly after reperfusion. Spontaneous firing rate was 0.47 ± 0.81 spikes/s (n = 34) before ischemia. No spontaneous firing was detected within 2 h after reperfusion, and the firing rate gradually returned to preischemic levels 2- 5 h after reperfusion (0.28 ± 0.96 spikes/s, n = 15). Neuronal hyperactivity as indicated by an increased spontaneous firing rate was not observed up to 7 h after reperfusion. 8. Stimulation of the contralateral commissural pathway elicited excitatory postsynaptic potentials (EPSPs) minutes after reperfusion, whereas inhibitory postsynaptic potentials (IPSPs) did not appear until °1 h after reperfusion. Within 2 h after reperfusion, the amplitudes of EPSPs slightly increased compared with those before ischemia, and the duration of EPSPs significantly increased from 18.00 ± 3.08 ms (n = 5) before ischemia to 26.83 ± 4.26 ms (n = 6, P <0.01). The amplitude and duration of EPSPs returned to preischemic levels 4-5 h after reperfusion. 9. Results from the present study indicate that the input resistance and time constant of CA1 pyramidal neurons decrease during cerebral ischemia. After 5 min of forebrain ischemia, the spontaneous neuronal activities, evoked synaptic potentials and excitability of CA1 neurons are transiently suppressed after reperfusion. No hyperactivity was observed up to 7 h after reperfusion.",
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N2 - 1. Electrophysiological changes of CA1 pyramidal neurons in rat hippocampus were studied before, during 5 min forebrain ischemia, and after reperfusion using in vivo intracellular recording and staining techniques. 2. Membrane input resistance of CA1 neurons decreased from 25.98 ± 7.24 MΩ (mean ± SD, n = 42) before ischemia to 16.33 ± 6.50 MΩ shortly after the onset of ischemia (n = 6, P <0.01). The input resistance fell to zero during ischemic depolarization and quickly returned to 24.42 ± 10.36 MΩ (n = 11) within 2 h after reperfusion. 3. The time constant of CA1 neurons decreased from 11.49 ± 5.45 ms (n = 36) to 3.09 ± 1.66 ms (n = 6, P <0.01) during ischemia. The time constant remained significantly less than preischemic levels within 2 h after reperfusion (5.40 ± 2.60 ms, n = 13, P <0.01) and gradually returned to preischemic levels 4-5 h after reperfusion. 4. The spike height decreased from 91 ± 10.35 mV (n = 45) before ischemia to 82 ± 8.00 mV (n = 9, P <0.05) within 2 h after reperfusion and fully returned to preischemic level 2-5 h after reperfusion. The spike width increased from 1.14 ± 0.22 ms (n = 45) before ischemia to 1.36 ± 0.22 ms (n = 9, P <0.05) within 2 h after reperfusion and remained at this level 4-5 h after reperfusion. 5. The spike threshold significantly increased from -54 ± 3.93 mV (n = 45) before ischemia to 49 ± 5.04 mV (n = 8, P <0.01) within 2 h after reperfusion. The rheobase increased accordingly from 0.34 ± 0.16 nA (n = 41) to 0.73 ± 0.26 nA (n = 6, P <0.01). The spike threshold returned to control levels 4-5 h after reperfusion, while the rheobase was still significantly higher than control levels (0.50 ± 0.21 nA, n = 16, P <0.01). 6. The frequency of repetitive firing evoked by depolarizing current pulses was suppressed within 2 h after reperfusion (n = 6, P <0.01). The spike frequency increased slightly 2-5 h after reperfusion but was still significantly below the control levels (n = 12, P <0.01). 7. Spontaneous synaptic activities ceased during ischemia and remained depressed shortly after reperfusion. Spontaneous firing rate was 0.47 ± 0.81 spikes/s (n = 34) before ischemia. No spontaneous firing was detected within 2 h after reperfusion, and the firing rate gradually returned to preischemic levels 2- 5 h after reperfusion (0.28 ± 0.96 spikes/s, n = 15). Neuronal hyperactivity as indicated by an increased spontaneous firing rate was not observed up to 7 h after reperfusion. 8. Stimulation of the contralateral commissural pathway elicited excitatory postsynaptic potentials (EPSPs) minutes after reperfusion, whereas inhibitory postsynaptic potentials (IPSPs) did not appear until °1 h after reperfusion. Within 2 h after reperfusion, the amplitudes of EPSPs slightly increased compared with those before ischemia, and the duration of EPSPs significantly increased from 18.00 ± 3.08 ms (n = 5) before ischemia to 26.83 ± 4.26 ms (n = 6, P <0.01). The amplitude and duration of EPSPs returned to preischemic levels 4-5 h after reperfusion. 9. Results from the present study indicate that the input resistance and time constant of CA1 pyramidal neurons decrease during cerebral ischemia. After 5 min of forebrain ischemia, the spontaneous neuronal activities, evoked synaptic potentials and excitability of CA1 neurons are transiently suppressed after reperfusion. No hyperactivity was observed up to 7 h after reperfusion.

AB - 1. Electrophysiological changes of CA1 pyramidal neurons in rat hippocampus were studied before, during 5 min forebrain ischemia, and after reperfusion using in vivo intracellular recording and staining techniques. 2. Membrane input resistance of CA1 neurons decreased from 25.98 ± 7.24 MΩ (mean ± SD, n = 42) before ischemia to 16.33 ± 6.50 MΩ shortly after the onset of ischemia (n = 6, P <0.01). The input resistance fell to zero during ischemic depolarization and quickly returned to 24.42 ± 10.36 MΩ (n = 11) within 2 h after reperfusion. 3. The time constant of CA1 neurons decreased from 11.49 ± 5.45 ms (n = 36) to 3.09 ± 1.66 ms (n = 6, P <0.01) during ischemia. The time constant remained significantly less than preischemic levels within 2 h after reperfusion (5.40 ± 2.60 ms, n = 13, P <0.01) and gradually returned to preischemic levels 4-5 h after reperfusion. 4. The spike height decreased from 91 ± 10.35 mV (n = 45) before ischemia to 82 ± 8.00 mV (n = 9, P <0.05) within 2 h after reperfusion and fully returned to preischemic level 2-5 h after reperfusion. The spike width increased from 1.14 ± 0.22 ms (n = 45) before ischemia to 1.36 ± 0.22 ms (n = 9, P <0.05) within 2 h after reperfusion and remained at this level 4-5 h after reperfusion. 5. The spike threshold significantly increased from -54 ± 3.93 mV (n = 45) before ischemia to 49 ± 5.04 mV (n = 8, P <0.01) within 2 h after reperfusion. The rheobase increased accordingly from 0.34 ± 0.16 nA (n = 41) to 0.73 ± 0.26 nA (n = 6, P <0.01). The spike threshold returned to control levels 4-5 h after reperfusion, while the rheobase was still significantly higher than control levels (0.50 ± 0.21 nA, n = 16, P <0.01). 6. The frequency of repetitive firing evoked by depolarizing current pulses was suppressed within 2 h after reperfusion (n = 6, P <0.01). The spike frequency increased slightly 2-5 h after reperfusion but was still significantly below the control levels (n = 12, P <0.01). 7. Spontaneous synaptic activities ceased during ischemia and remained depressed shortly after reperfusion. Spontaneous firing rate was 0.47 ± 0.81 spikes/s (n = 34) before ischemia. No spontaneous firing was detected within 2 h after reperfusion, and the firing rate gradually returned to preischemic levels 2- 5 h after reperfusion (0.28 ± 0.96 spikes/s, n = 15). Neuronal hyperactivity as indicated by an increased spontaneous firing rate was not observed up to 7 h after reperfusion. 8. Stimulation of the contralateral commissural pathway elicited excitatory postsynaptic potentials (EPSPs) minutes after reperfusion, whereas inhibitory postsynaptic potentials (IPSPs) did not appear until °1 h after reperfusion. Within 2 h after reperfusion, the amplitudes of EPSPs slightly increased compared with those before ischemia, and the duration of EPSPs significantly increased from 18.00 ± 3.08 ms (n = 5) before ischemia to 26.83 ± 4.26 ms (n = 6, P <0.01). The amplitude and duration of EPSPs returned to preischemic levels 4-5 h after reperfusion. 9. Results from the present study indicate that the input resistance and time constant of CA1 pyramidal neurons decrease during cerebral ischemia. After 5 min of forebrain ischemia, the spontaneous neuronal activities, evoked synaptic potentials and excitability of CA1 neurons are transiently suppressed after reperfusion. No hyperactivity was observed up to 7 h after reperfusion.

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