Integration of Wing Proprioceptive and Descending Exteroceptive Sensory Inputs by Thoracic Interneurones of the Locust

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Abstract
The campaniform sensilla on the wings of the locust are strain-sensitive mechanoreceptors that provide proprioceptive feedback about wing forces, particularly aerodynamic lift, experienced during flight. They can be excited by imposed deformations of the wing, including those caused by imposed wing twisting. The afferents of the single subcostal group of sensilla on the hindwing had the same directional selectivity for supinating twist and shared the properties of a dynamic sensitivity and adaptation. A group of strain-sensitive mechanoreceptors with similar properties, presumably campaniform sensilla, is also found in the forewings. Four types of thoracic interneurones influenced by these factors were recorded and stained intracellularly. The response of interneurone 5AA to imposed deformations of the hindwing ipsilateral to its soma is determined by excitatory chemical synaptic input from the campaniform sensilla. Interneurone and sensilla have a common directional selectivity and optimal stimulus, and similar qualitative dynamics of response. Each spike of individual afferents is followed at short, constant latency by an excitatory postsynaptic potential (EPSP) in the interneurone, even at instantaneous frequencies of about 90 Hz. Physiological evidence is consistent with direct, chemically mediated synaptic inputs from campaniform sensilla afferents. Interneurone 5AA is also excited by a short-latency, chemical synaptic input from the ocelli when lights are turned off. EPSPs could be elicited by light-off stimuli to the median and contralateral, but not the ipsilateral, ocelli. In addition, the interneurone is excited when the head is moved relative to the thorax. The other three interneurones respond to strains in more than one wing. Inputs are derived from specific combinations of wings, with the sign of response depending on the neurone and the particular wing. Interneurones 3AA and 1AA are also phasically excited by light-off stimuli. In 1AA this response was shown to originate from the ocelli. Median and contralateral, but not ipsilateral, ocelli could evoke EPSPs. This neurone was also excited by imposed head movements. It is argued that the interneurones described here at suited to monitor lift production in particular wings and its pattern among several wings. Convergence of ocellar and head-motion inputs implies a function in the exteroceptive detection and correction of flight instability. It is inferred that these thoracic interneurones may act as the nexus for several different feedback pathways, proprioceptive and exteroceptive, which modulate flight motor output.