Journal of Neurophysiology, Vol 76, Issue 3 1689-1697, Copyright © 1996 by APS

ARTICLES

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

Z. C. Xu and W. A. Pulsinelli
Department of Neurology, University of Tennessee, Memphis 38163, USA.

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 M omega (mean +/- SD, n = 42) before ischemia to 16.33 +/- 6.50 M omega 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 M omega (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 approximately 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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