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Synaptically Activated Cl^– Accumulation Responsible for Depolarizing GABAergic Responses in Mature Hippocampal Neurons

¹ Department of System Neuroscience, Tokyo Metropolitan Institute for Neuroscience, Fuchu, Tokyo 183-8526, Japan ² The Japan Society for the Promotion of Science, Tokyo 102-8471, Japan ³ Department of Physiology, Hamamatsu University School of Medicine, Hamamatsu, Shizuoka 431-3192, Japan ⁴ First Department of Medicine, Hamamatsu University School of Medicine, Hamamatsu, Shizuoka 431-3192, Japan ⁵ Biological Information Processing, Graduate School of Electronic Science and Technology, Shizuoka University, Hamamatsu, Shizuoka 432-8011, Japan

Submitted 14 February 2003; accepted in final form 20 May 2003

It is known that GABA, a major inhibitory transmitter in the CNS, acts as an excitatory (or depolarizing) transmitter transiently after intense GABA_A receptor activation in adult brains. The depolarizing effect is considered to be dependent on two GABA_A receptor-permeable anions, chloride (Cl^–) and bicarbonate (HCO₃^–). However, little is known about their spatial and temporal profiles during the GABAergic depolarization in postsynaptic neurons. In the present study, we show that the amplitude of synaptically induced depolarizing response was correlated with intracellular Cl^– accumulation in the soma of mature hippocampal CA1 pyramidal cells, by using whole cell patch-clamp recording and Cl^– imaging technique with a Cl^– indicator 6-methoxy-N-ethylquinolinium iodide (MEQ). The synaptically activated Cl^– accumulation was mediated dominantly through GABA_A receptors. Basket cells, a subclass of fast-spiking interneurons innervating the somatic portion of the pyramidal cells, actually fired at high frequency during the Cl^– accumulation accompanying the depolarizing responses. These results suggest synaptically activated GABA_A-mediated Cl^– accumulation may play a critical role in generation of an excitatory GABAergic response in the mature pyramidal cells receiving intense synaptic inputs. This may be the first demonstration of microscopic visualization of intracellular Cl^– accumulation during synaptic activation.

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