The non-impulsive stretch-receptor complex of the crab: a study of depolarization-release coupling at a tonic sensorimotor synapse

Abstract

A new preparation for the study of synaptic transmission is described from the thoracic ganglion of the crabCallinectes sapidus. The central anatomy of the nonimpulsive stretch-receptor neurons of the thoracic-coxal joint and that of the promotor motoneurons with which they form synaptic junctions was studied with intracellular cobalt staining and light and electron microscopy. Attention was centred on the interaction of the stretch-receptor T-fibre and the four large motoneurons supplying the promotor muscle which have their cell-bodies on the dorsal surface of the ganglion. The presynaptic terminal region of the T-fibre appeared to be a simple cylinder in form with a diameter of 40-60 μm and containing large stores of synaptic vesicles at its periphery, opposite the complex of motoneuron dendrites. The transmission characteristics of the junctions between receptor cell and motoneurons were studied by transmembrane current injection into the isolated T-fibre by means of a sucrose gap and simultaneous intracellular recording with microelectrodes from the presynaptic terminal and the somata of postsynaptic cells. It was shown that depolarization-release coupling in the T-fibre has similar properties to those that have been demonstrated in the squid giant synapse, with the same values for ‘threshold’, peak release and ‘suppression potential’. The crab synapses differ from that of the squid in that they normally transmit prolonged, graded depolarizations (i.e. receptor potentials) which are decrementally conducted from the periphery. Consistent with this role, the junctions were found to be capable of continuous tonic transmission over many seconds without the strong depletion seen in more phasic synapses. In a study of the relation between the synaptic properties and the stretch reflex it was shown that some of the time- and amplitude-dependent behaviour of the overall reflex can be encoded at the level of the synaptic transmission, largely through the parameter of transmitter availability. Conduction of electrical signals in the proximal and presynaptic part of the sensory fibre was also investigated. Transient responses to step depolarizing currents in the fibre indicate the existence of a mechanism for the partial compensation of capacitative distortion in the decrementally conducted receptor potential. This is the first example of intracellular recording from presynaptic terminals of nonimpulsive neurons with simultaneous monitoring of postsynaptic potential changes, allowing for a direct analysis of depolarization-release coupling characteristics. The use of the preparation for further study of synaptic physiology and sensorimotor systems is discussed.