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J Neurophysiol 85: 2166-2176, 2001;
0022-3077/01 $5.00
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The Journal of Neurophysiology Vol. 85 No. 5 May 2001, pp. 2166-2176
Copyright ©2001 by the American Physiological Society

Post-Episode Depression of GABAergic Transmission in Spinal Neurons of the Chick Embryo

Nikolai Chub and Michael J. O'Donovan

Section on Developmental Neurobiology, Laboratory of Neural Control, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892

Chub, Nikolai and Michael J. O'Donovan. Post-Episode Depression of GABAergic Transmission in Spinal Neurons of the Chick Embryo. J. Neurophysiol. 85: 2166-2176, 2001. Whole cell recordings were obtained from ventral horn neurons in spontaneously active spinal cords isolated from the chick embryo [embryonic days 10 to 11 (E10-E11)] to examine the post-episode depression of GABAergic transmission. Spontaneous activity occurred as recurrent, rhythmic episodes approximately 60 s in duration with 10- to 15-min quiescent inter-episode intervals. Current-clamp recording revealed that episodes were followed by a transient hyperpolarization (7 ± 1.2 mV, mean ± SE), which dissipated as a slow (0.5-1 mV/min) depolarization until the next episode. Local application of bicuculline 8 min after an episode hyperpolarized spinal neurons by 6 ± 0.8 mV and increased their input resistance by 13%, suggesting the involvement of GABAergic transmission. Gramicidin perforated-patch recordings showed that the GABAa reversal potential was above rest potential (EGABAa = -29 ± 3 mV) and allowed estimation of the physiological intracellular [Cl-] = 50 mM. In whole cell configuration (with physiological electrode [Cl-]), two distinct types of endogenous GABAergic currents (IGABAa) were found during the inter-episode interval. The first comprised TTX-resistant, asynchronous miniature postsynaptic currents (mPSCs), an indicator of quantal GABA release (up to 42% of total mPSCs). The second (tonic IGABAa) was complimentary to the slow membrane depolarization and may arise from persistent activation of extrasynaptic GABAa receptors. We estimate that approximately 10 postsynaptic channels are activated by a single quantum of GABA release during an mPSC and that about 30 extrasynaptic GABAa channels are required for generation of the tonic IGABAa in ventral horn neurons. We investigated the post-episode depression of IGABAa by local application of GABA or isoguvacine (100 µM, for 10-30 s) applied before and after an episode at holding potentials (Vhold) -60 mV. The amplitude of the evoked IGABA was compared after clamping the cell during the episode at one of three different Vhold: -60 mV, below EGABAa resulting in Cl- efflux; -30 mV, close to EGABAa with minimal Cl- flux; and 0 mV, above EGABAa resulting in Cl- influx during the episode. The amplitude of the evoked IGABA changed according to the direction of Cl- flux during the episode: at -60 mV a 41% decrease, at -30 mV a 4% reduction, and at 0 mV a 19% increase. These post-episode changes were accompanied by shifts of EGABAa of -10, -1.2, and +7 mV, respectively. We conclude that redistribution of intracellular [Cl-] during spontaneous episodes is likely to be an important postsynaptic mechanism involved in the post-episode depression of GABAergic transmission in chick embryo spinal neurons.




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