Rapid activation of GABAergic interneurons and possible calcium independent GABA release in the mormyrid electrosensory lobe

Rapid activation of GABAergic interneurons and possible calcium independent GABA release in the mormyrid electrosensory lobe. J. Neurophysiol. 83: 159 2-1604, 2000. The primary efferent fibers from the electroreceptors of morm yrid electric fish terminate centrally in the granular layer of the electro sensory lobe (ELL). This study examines the excitatory and inhibitory proce sses that take place in this layer using an in vitro slice preparation and field potentials evoked by stimulation of primary afferent fibers in the de ep fiber layer of ELL. The postsynaptic response to stimulation of the affe rent fibers was still present after blocking chemical transmission in three different ways: by adding glutamate receptor antagonists to the medium, by substituting a nominally calcium-free medium for normal medium, and by blo cking calcium channels with cadmium. Blockade of chemical transmission was demonstrated by disappearance of control responses to parallel fiber stimul ation. The continued presence of a postsynaptic response in the absence of chemical excitation is consistent with previous anatomic and physiological evidence for electrical synapses between afferent fibers and granular cells in ELL. Granular cell activation by primary afferent fibers was followed b y a powerful, short-latency inhibition mediated by GABA and GABA(A) recepto rs, as indicated by a large increase in the postsynaptic response to affere nt fiber stimulation following application of the GABA(A) receptor antagoni st, bicuculline. Bicuculline caused a marked increase of the postsynaptic r esponse even after chemical synaptic excitation had been blocked by glutama te receptor antagonists, by a calcium-free medium, or by cadmium. Thus acti vation of the inhibitory interneurons responsible for GABA release did not require chemical excitation. Nonchemical excitation of the inhibitory inter neurons could be mediated either by electrical synapses between afferent fi bers and inhibitory interneurons, or by nonsynaptic activation of the large GABAergic terminals that are known to be present on granular cells. The ma rked increase of the postsynaptic response caused by bicuculline in a calci um-free medium or in the presence of cadmium suggests that the release of G ABA by inhibitory terminals was not entirely dependent on calcium influx. T his effect of bicuculline on the postsynaptic response in a calcium-free me dium or in the presence of cadmium was markedly reduced by prior addition o f the GABA transporter antagonist, nipecotic acid. Thus calcium-independent release of GABA may occur in ELL and may be partly dependent on reversal o f a GABA transporter. Rapid and powerful inhibition at the first stage in t he processing of electrosensory information could serve to enhance the smal l differences in latency among afferent fibers that appear to encode small differences in stimulus intensity.