Journal of Neurophysiology, Vol 56, Issue 1 99-122, Copyright © 1986 by APS

ARTICLES

Ephaptically generated potentials in CA1 neurons of rat's hippocampus in situ

C. C. Yim, K. Krnjevic and T. Dalkara

Passive (ephaptic) transmembrane currents generated by antidromically evoked electrical fields were studied in CA1 hippocampal neurons of urethan-anesthetized rats. Recording was mostly from the stratum pyramidale where the fields have a maximum (negative) amplitude. The antidromic population spike was consistently smaller when recorded inside a noninvaded neuron rather than extracellularly. This indicated a substantial transmembrane potential (Vm), which was revealed and quantified by subtracting from the intracellular record a just-extracellular one. In neurons that have spikes greater than or equal to 40 mV (mean 60 mV), the average Vm was 41.1% of the extracellular field (Ve; mean 6.7 mV). Typically, Vm was very brief (mean duration 1.1 ms), predominantly monophasic, and in a depolarizing direction. Though almost synchronous with Ve, the peak of Vm was most often delayed slightly. Its amplitude varied with the intensity of antidromic stimulation, bearing an approximately constant relation to Ve, and it was not markedly sensitive to large changes in membrane potential. Most of these features confirm its ephaptic nature. By contrast, no consistent Vm was recorded from unresponsive cells, presumed to be glia. When combined with subthreshold depolarizing pulses, antidromic fields increased the firing probability of cells not activated by the antidromic stimulus. The ephaptic nature of this excitation was indicated by its very short latency, too early to be of synaptic origin, a much greater jitter of spike latency than was seen with antidromic spikes, and its inability to follow repetitive stimulation at frequencies as low as 2 Hz. In addition, juxta-threshold ephaptic excitations showed the random patterns of firing and very steep relation to intensity of stimulation expected of single-unit responses to electrical stimulation. In general, much larger excitatory effects could be demonstrated in neurons that had a high threshold for antidromic activation. The correlation between Vm and the increase in firing probability (r = 0.85) was strongly positive. A significant excitatory effect was detectable with antidromic fields as small as 1 mV. These ephaptically generated transmembrane potentials are probably of functional significance, even under physiological conditions, particularly in promoting synchronized firing of CA1 neurons. In the APPENDIX, the predictions of a simple neuronal model as a lumped resistance and capacitance circuit are shown to agree quite well with the observations.(ABSTRACT TRUNCATED AT 400 WORDS)

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