Slow and fast synaptic inhibition evoked by pattern-generating neurons of the gastric mill network in spiny lobsters

Abstract

1. In this paper we begin an assessment of the role of synaptic properties, especially synaptic time course, in the function of the central pattern generator circuit (CPG) that controls rhythmic movements of the gastric mill in the foregut of spiny lobster (Panulirus interruptus). 2. The majority of neurons in the gastric CPG are motor neurons (MNs) that innervate striated muscles of the gastric mill but that also make electrical and inhibitory chemical interconnections within the neuropil of the stomatogastric ganglion. We studied the ionic dependence, pharmacology, and time course of inhibitory postsynaptic potentials (IPSPs) evoked by two such MNs, the dorsal gastric (DG) and lateral gastric (LG), in their central synaptic partners. In the periphery, LG and DG are thought to release glutamate. 3. LG and DG evoke two types of IPSPs in follower neurons. The first, fast type of IPSP rises rapidly (the graded component within 100-300 ms, the spike-mediated components within a few tens of ms), is mediated by increased chloride and potassium conductances, and is blocked by < or = 10 microM picrotoxin (PTX). These fast IPSPs closely resemble the glutamatergic IPSPs described in the pyloric circuit of the same ganglion. 4. The second, slow type of IPSP has a long rise time (1-2 s), is mediated by increased conductance to potassium (with little or no involvement of chloride), and is not blocked by 10 microM PTX, 5 mM tetraethylammonium chloride, or 0.1 mM scopolamine. These properties distinguish slow IPSPs from the forms of glutamatergic and cholinergic inhibition that have been described in the pyloric circuit. 5. Fast inhibition occurs alone at connections from DG and LG to power stroke MNs (median gastric and gastric mill). Slow inhibition occurs in parallel with fast inhibition (producing dual-component responses) at connections from LG to return stroke neurons [lateral posterior gastric MNs, (LPGs) and interneuron 1]. DG seems to evoke only a slow IPSP in LPGs. 6. The transmitter mediating the fast IPSPs is likely to be glutamate. We discuss possible mechanisms for the slow IPSP but have no evidence at present concerning the transmitter(s) involved. Slow inhibition is likely to be an important synaptic "building block" in the gastric CPG; it is "tuned" to the duration of gastric bursts and may contribute to the long cycle period of gastric rhythms.