Presynaptic Depolarization Mediates Presynaptic Inhibition at a Synapse Between An Identified Mechanosensory Neurone and Giant Interneurone 3 in the First Instar Cockroach, Periplaneta Americana

Abstract

Intracellular microelectrodes were used to study presynaptic inhibition at a cholinergic synapse between identified neurones: the lateral filiform hair sensory neurone (LFHSN) and giant interneurone 3 (GI3) in the terminal ganglion of the first instar cockroach Periplaneta americana. The LFHSN-GI3 synapse was shown to fulfil physiological criteria for monosynaptic transmission: the latency of the EPSPs was 1.4 ms and was constant during high-frequency firing of LFHSN; transmission was progressively and reversibly abolished by replacement of Ca2+ with Mg2+. Movement of the lateral filiform hair towards the cereal tip produced a burst of spikes in LFHSN and a burst of EPSPs in GI 3. Movement of the medial filiform hair towards the base of the cercus produced a burst of spikes in the medial filiform hair sensory neurone (MFHSN) and a burst of EPSPs in GI 2. EPSPs evoked in GI 3 by LFHSN spikes were inhibited during bursts of EPSPs in GI 2 which were evoked by MFHSN spikes. LFHSN was depolarized and its spikes were reduced in amplitude during spike bursts in MFHSN. Reduction in LFHSN spike amplitude reduced GI 3 EPSPs. This phenomenon was attributed, therefore, to presynaptic inhibition. The occurrence of presynaptic inhibition was dependent upon the degree of delayed rectification exhibited by the LFHSN axon. Hyperpolarization of LFHSN increased spike height, but did not increase the amplitude of GI 3 EPSPs. The delay between the onset of MFHSN-evoked EPSPs in GI 2 and MFHSNevoked depolarizations in LFHSN suggested that MFHSN does not synapse directly onto LFHSN. Neither depolarization nor hyperpolarization of GI 2 had any effect on MFHSN-mediated presynaptic inhibition of LFHSN-GI 3 transmission, therefore it was considered unlikely that GI 2 synapses onto LFHSN. Prolonged hyperpolarization lowered the LFHSN spike threshold and temporarily abolished presynaptic inhibition. Bursts of spikes in LFHSN mediated presynaptic inhibition of MFHSN-GI2 EPSPs. Mutual presynaptic inhibition by the FHSNs may have a functional significance in sharpening the boundaries of the GIs' directional sensitivities.