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Volume 17, Number 20, Issue of October 15, 1997 pp. 7662-7672
Copyright ©1997 Society for Neuroscience

Long-Lasting GABA-Mediated Depolarization Evoked by High-Frequency Stimulation in Pyramidal Neurons of Rat Hippocampal Slice Is Attributable to a Network-Driven, Bicarbonate-Dependent K+ Transient

Received May 12, 1997; revised July 21, 1997; accepted Aug. 5, 1997.

Kai Kaila, Karri Lamsa, Sergei Smirnov, Tomi Taira, and Juha Voipio

Department of Biosciences, Division of Animal Physiology, University of Helsinki, FIN-00014 Helsinki, Finland

Biphasic GABAA-mediated postsynaptic responses can be readily evoked in CA1 pyramidal neurons of rat hippocampal slices by high-frequency stimulus (HFS) trains in the presence of ionotropic glutamate receptor antagonists. In the present experiments with sharp microelectrodes, whole-cell techniques, and K+-selective microelectrodes, an HFS train (40 pulses at 100 Hz) applied in stratum radiatum close to the recording site evoked a brief hyperpolarizing IPSP (hIPSP), which turned into a prolonged (2-3 sec) depolarization (<UNL>G</UNL>ABA-mediated <UNL>d</UNL>epolarizing <UNL>p</UNL>ostsynaptic <UNL>p</UNL>otential; GDPSP). The I-V relationships of the postsynaptic currents (hIPSC and GDPSC) had distinct characteristics: the hIPSC and the early GDPSC showed outward rectification, whereas the late GDPSC was reduced with positive voltage steps to zero or beyond (inward rectification), but often no clear reversal was seen. That two distinct currents contribute to the generation of the GDPSP was also evident from the finding that a second HFS train at peak or late GDPSP induced a prompt GABAA-mediated hyperpolarization. The GDPSP/C was dependent on the availability of bicarbonate, but not on interstitial or intrapyramidal carbonic anhydrase activity.

The HFS train evoked a rapid GABAA-mediated bicarbonate-dependent increase in the extracellular K+ concentration ([K+]o), and the GDPSP followed the K+ transient in a sub-Nernstian manner. The spatial and pharmacological characteristics of the [K+]o shift indicated that it is generated by a local network of GABAergic interneurons. The brief ascending phase of the GDPSP is linked to a K+-dependent accumulation of intracellular Cl-. Thereafter, a nonsynaptic mechanism, a direct depolarizing effect of the [K+]o shift, is responsible for the most conspicuous characteristics of the GDPSP: its large amplitude and prolonged duration.

Key words: GABAA receptor; postsynaptic depolarization; bicarbonate; potassium; hippocampal pyramidal neuron; inhibitory network; glial depolarization




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