Parallel processing of proprioceptive signals by spiking local interneurons and motor neurons in the locust

Abstract

The connections made by afferents from a proprioceptor at the femorotibial joint in a hind leg of a locust, the femoral chordotonal organ (FCO), were determined by making intracellular recordings from motor neurons and spiking local interneurons in the central nervous system and from afferent cell bodies in the periphery. Staining the central projections of the afferent neurons with dye introduced into their axons at the receptor, and the intracellular injection of dye into motor neurons and interneurons, shows that the branches of all 3 types of neuron overlap in specific regions of neuropile. Afferents excited by a movement of the receptor apodeme that is equivalent to an imposed extension of the femorotibial joint excite flexor tibiae motor neurons and some spiking local interneurons with cell bodies at the ventral midline of the metathoracic ganglion. The opposite movement excites extensor tibiae motor neurons and a different set of spiking local interneurons. Spikes in afferents that excite flexor motor neurons evoke depolarizing potentials that follow each spike with a consistent central latency of approximately 1.5 msec. The amplitude of the depolarizing potentials is dependent upon the membrane potential of the motor neuron. This evidence points to the connection being direct and to the potentials' being EPSPs. Simultaneous recordings from certain spiking local interneurons and certain flexor motor neurons show that they receive many synaptic potentials in common and are driven in a parallel fashion by movements of the receptor apodeme. Spikes of some afferents evoke EPSPs in both neurons with the same consistency and latency. An afferent can therefore synapse directly upon a motor neuron and a spiking local interneuron. Each afferent synapses on several motor neurons and possibly upon several interneurons. In turn, each motor neuron and each interneuron receives inputs from several afferents.