This paper, the first in a series concerning the neurobiology of sensory cilia, describes the ultrastructure of our chosen model system – the proximal femoral chordotonal organ (FCO) in pro-and mesothoracic grasshopper legs. The FCO is a bundle of 150–200 longitudinally oriented chordotonal sensilla. Each chordotonal sensillum is a mechano-receptive unit that contains two bipolar neurons whose dendrites bear sensory cilia. The structure of the sensory cilia leads us to suggest that they are motile cilia that respond to the mechanical stimulus with an “active stroke” which excites a transducer membrane at the dendrite tip.

This paper describes the ultrastructural modifications that cockroach campaniform sensilla undergo at three major stages in the molting cycle and finds that the sensilla are physiological functional at all developmental stages leading to ecdysis. Late stage animals on the verge of ecdysis have two completely separate cuticles. The campaniform sensillum sends a 220-mum extension of the sensory process through a hole in its cap in the new (inner) cuticle across a fluid-filled molting space to its functional insertion in the cap in the old (outer) cuticle. Mechanical stimulation of the old cap excites the sensillum. The ultrastructural geometry of late stage sensilla, coupled with the observation they are physiolgically functional, supports the hypotheses (a) that sensory transduction occurs at the tip of the sensory process, and (b) that cap identation causes the cap cuticle to pinch the tip of the sensory process, thereby stimulating the sensillum.

Combined high-voltage electron-microscopic and electrophysiological studies strongly suggest that cilia play an active role in sensory transduction in the grasshopper proximal femoral chordotonal organ (FCO) a ciliated mechanoreceptor. The FCO of proand mesothoracic legs of Melanoplus bivittatus contains a group of several hundred chorodontal sensilla arranged in a near-parallel bundle and slung between the proximal femur and the knee joint. Both flexion and extension of the tibia stimulate the FCO, which appears to measure the femoro-tibial angle. The FCO’s U-shaped response curve indicates that progressive flexion or extension from the resting joint angle of 90 degrees increases the response frequency of individual receptors and recruits additional units as well. Since the FCO is a purely tonic mechanoreceptor, it is possible to fix FCOs during maximum and minimum states of stimulation and electron-microscopically observed changes in the receptor’s fine structure. The most conspicuous change is the production of a pronounced bend at the base of the sensory cilia in chordotonal sensilla of maximally stimulated femoral chordotonal organs.