Ocellar Input to the Flight Motor System of the Locust: Structure and Function

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Abstract
This paper deals with the physiology, anatomy and function of the following classes of neurones in the locust Schistocerca: (a) neurones carrying ocellar information to the pterothorax (Descending Ocellar Neurones, DONs), (b) mesothoracic Flight Motor Neurones (FMNs), (c) a heterogenous class of inter- and intraganglionic thoracic interneurones which receive input from the DONs, here called Thoracic Ocellar Interneurones (TONs) without prejudice to their other possible inputs and functions. The thoracic arborizations of five different DONs are characterized. All project unilaterally to the pterothorax, four out of five to the ipsilateral mesothoracic or meso- and metathoracic ganglia. All are phasic OFF units, responding to stimulation either of one lateral ocellus or of the medial ocellus or of both, but none responded to the cephalic wind-hairs. Four of the five DONs showed no response decrement at stimulus frequencies up to 80 Hz. One showed habituation, recovery during a rest interval, and dishabituation in response to mechanical stimulation of a leg. There are more than six DONs, probably more than ten, in each connective. All types of recorded mesothoracic FMNs receive monosynaptic EPSPs from the DONs and/or delayed IPSPs (presumably via TONs) in at least some animals. The pattern of connection is compatible with the hypothesis that a roll or downward pitch deviation induces compensating movements of the wings to correct the deviation. Many of these DON/FMN connections were, however, only occasionally recorded. None of the ocellar EPSPs recorded in the FMNs elicited spikes. Most TONs receive monosynaptic EPSPs from one or more DONs, sometimes causing them to spike. Two receive delayed IPSPs, presumably via other TONs. At least one third of the recorded TONs spike in phase with either elevator or depressor FMNs during stimulated flight. Intraganglionic TONs in the mesothorax are all unilateral. Their anatomy suggests that they distribute input from DONs to various combinations of ipsilateral FMNs. Interganglionic TONs can be either unilateral or bilateral in the mesothoracic ganglion, and project unilaterally to the metathoracic (or rarely the prothoracic) ganglion, where at least one makes inhibitory synapses with a FMN. Phasic ocellar information reaches the FMNs by two routes. One produces fast subthreshold PSPs in the FMNs directly. The other produces spikes and PSPs in thoracic interneurones, at least some of which are phasically active during flight and are presynaptic to FMNs. The roles of the two pathways are discussed.