Influence of temperature on anoxic responses of neocortical pyramidal neurons

Abstract

Intracellular recordings were made in pyramidal neurons of layers II–III of rat fronto-parietal neocortical slices. The membrane and synaptic properties and effects of brief (4–6 min) anoxia—anoxic depolarization and synaptic depression—were recorded at temperatures between 26 and 37.5°C. In normoxic conditions, both warming (⩾ 35°C) and cooling (⩽ 32°C) induced a reduction in the amplitude of early and late excitatory postsynaptic potentials and abolished inhibitory postsynaptic potentials. Excitatory postsynaptic potential latency decreased with warming and increased with cooling. Warming also induced spontaneous brief depolarizations, had a general slow depolarizing effect on resting membrane potential, and decreased input resistance. During oxygen deprivation, the steepness of the rising phase of the anoxic depolarization and the duration of the repolarization phase were augmented by warming above 36.5°C (3.7 ± 0.1 vs1.9 ± 0.1mV/min and8.75 ± 0.98 vs4.16 ± 0.28min, respectively). The peak amplitude of the anoxic depolarization increased in only one-third of trials (6.6 ± 0.6 vs4.3 ± 0.4mV). Warming potentiated the depressant effect of anoxia: at 36.5°C early excitatory postsynaptic potential amplitude decreased to32.3 ± 5.2% of control compared with58.3 ± 1.2% at 33.5°C, the late excitatory postsynaptic potential was abolished in < 2 min, and the recovery of the compound excitatory postsynaptic potential was prolonged (12.8 ± 0.8 vs7.8 ± 0.3min). Cooling reduced the amplitude of the anoxic depolarization and increased the input resistance. At 30.5–31°C there was a delay and diminution of the reduction of early excitatory postsynaptic potential amplitude (86.5 ± 3.8 vs 59.8 ± 4.3% of control at 33.5°C) and more rapid postanoxic recovery (4.2 ± 1.3 vs8.0 ± 1.1min). At 26°C excitatory postsynaptic potentials and resting membrane potential were unaffected by anoxia. These findings suggest that membrane and especially synaptic properties of neocortical neurons in vitro are optimally studied in this type of preparation at ≈ 34°C. In anoxic conditions, the effect of warming (⩾ 35°C) accentuates synaptic depression and to some extent the anoxic depolarization. Cooling has a stabilizing effect on membrane potential and protects against synaptic depression.