Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus)

The responses of two types of projection neurons of the electrosensory lateral line lobe, basilar (BP) and nonbasilar (NBP) pyramidal cells, to stimulation of primary electrosensory afferents were determined in the weakly electric fish, Apteronotus leptorhynchus. Using dyes to identify cell type, the response of NBP cells to stimulation of primary afferents was inhibitory, whereas the response of BP cells was excitation followed by inhibition. gamma-Aminobutyric acid (GABA) applications produced biphasic (depolarization then hyperpolarization) responses in most cells. GABA(A) antagonists blocked the depolarizing effect of GABA and reduced the hyperpolarizing effect. The GABA(B) antagonists weakly antagonized the hyperpolarizing effect. The early depolarization had a larger increase in cell conductance than the late hyperpolarization. The conductance changes were voltage dependent, increasing with depolarization. In both cell types, baclofen produced a slow small hyperpolarization and reduced the inhibitory postsynaptic potentials (IPSPs) evoked by primary afferent stimulation. Tetanic stimulation of primary afferents at physiological rarest (100-200 Hz) produced strongly summating compound IPSPs (similar to 500-ms duration) in NBP cells, which were usually sensitive to GABA(A) but not GABA(B) antagonists; in some cells there remained a slow IPSP that was unaffected by GABA(B) antagonists. BP cells responded with excitatory or mixed excitatory + inhibitory responses. The inhibitory response had both a fast (similar to 30 ms, GABA(A)) and longlasting slow phase (similar to 800 ms, mostly blocked by GABA(A) antagonists). In some cells there was a GABA(A) antagonist-insensitive slow IPSP (similar to 500 ms) that was sensitive to GABA(B) antagonists. Application of glutamate ionotropic receptor antagonists blocked the inhibitory response of NBP cells to primary afferent stimulation and the excitatory response of BP cells but enhanced the BP cell slow IPSP; this remaining slow IPSP was reduced by GABA(B) antagonists. Unit recordings in the granule cell layer and computer simulations of pyramidal cell inhibition suggested that the duration of the slow GABA(A) inhibition reflects the prolonged firing of GABAergic granule cell interneurons to primary afferent input. Correlation of the results with known GABAergic circuitry in the electrosensory lobe suggests that the GABAergic type 2 granule cell input to both pyramidal cell types is via GABA(A) receptors. The properties of the GC2 GABA(A) input are well suited to their putative role in gain control, regulation of phasicness, and coincidence detection. The slow GABA(B) IPSP evoked in BP cells is likely due to ovoid cell input to their basal dendrites.