Plasticity and proprioception in insects. I. Responses and cellular properties of individual receptors of the locust metathoracic femoral chordotonal organ.

The metathoracic femoral chordotonal organ is a joint angle receptor of the locust hindleg. It consists of 45-55 bipolar sensory neurones located distally in the femur and mechanically coupled to the tibia. Responses of receptors of the organ were examined by extracellular and intracellular recording. The organ as a whole encodes the angle of the femorotibial joint but shows substantial hysteresis. Tonic activity is greatest at the extremes of joint position. The organ possesses no direct linkage to tibial muscle fibres and shows no response to resisted muscle contractions in most ranges of joint angle. However, responses to extensor muscle contractions are obtained when the tibia is held in full flexion due to specializations of the femoro-tibial joint. These responses could be of importance in signalling preparedness for a jump. Intracellular soma recordings of activity in individual receptors indicate that the organ contains two types of receptors: phasic units that respond to joint movement and tonic units that encode joint position and also show some response to movement. All units are directionally sensitive and respond only in limited ranges of joint angle. Some phasic units increase firing frequency with increasing rate of movement and thus encode joint velocity. Other phasic units fire only single action potentials and can encode only the occurrence and direction of joint movement. All tonic units increase activity in the extremes of joint position and show substantial hysteresis upon return to more median positions. Direct soma depolarization produces different responses in different types of units: phasic receptors show only transient discharges to current injection; tonic receptors exhibit sustained increases in activity that are followed by periods of inhibition of background firing upon cessation of current injection. Receptors of the chordotonal organ are separable into two major groups, based upon their response characteristics, soma location and dendritic orientation: a dorsal group of receptors contains tonic units that respond in ranges of joint flexion (joint angle 0-80 degrees) and phasic units that respond to flexion movements; a ventral group of sensilla contains tonic units active in ranges of joint extension (joint angle 80-170 degrees) and phasic receptors that respond to extension movements. The response properties of these receptors are discussed with reference to the potential functions of the chordotonal organ in the locust's behavioural repertoire.