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Plasticity and Proprioception in Insects I

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Plasticity and Proprioception in Insects I J. exp. Biol. 116, 435-461 (1985) 435 Printed in Great Britain © The Company of Biologists Limited 1985 PLASTICITY AND PROPRIOCEPTION IN INSECTS I. RESPONSES AND CELLULAR PROPERTIES OF INDIVIDUAL RECEPTORS OF THE LOCUST METATHORACIC FEMORAL CHORDOTONAL ORGAN BY SASHA N. ZILL* Department of Biology, University of Oregon, Eugene, Oregon 97403, U.SA.. Accepted 12 October 1984 SUMMARY 1. 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. 2. Responses of receptors of the organ were examined by extracellular and intracellular recording. The organ as a whole encodes the angle of the femoro- tibial joint but shows substantial hysteresis. Tonic activity is greatest at the extremes of joint position. 3. 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. 4. 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. 5. 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. 6. 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. 7. 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°) and phasic units that respond to •Present address: Department of Anatomy, University of Colorado Medical School, Denver, Colorado 80262, U.S.A. Key words: Joint angle receptors, proprioception, cellular physiology. 436 S. N. ZILL flexion movements; a ventral group of sensilla contains tonic units active in ranges of joint extension (joint angle 80-170°) and phasic receptors that respond to extension movements. 8. The response properties of these receptors are discussed with reference to the potential functions of the chordotonal organ in the locust's behavioural repertoire. INTRODUCTION Many sense organs, in both vertebrates and invertebrates, precisely monitor the angles of joints of appendages (Granit, 1955; Mill, 1976). While the responses of joint angle receptors of vertebrates have been studied in detail (Boyd & Roberts, 1953; Ferrell, 1977), little is known about how information provided by these receptors is incorporated into behaviour (Grigg, Harrigan & Fogarty, 1978; Baxendale & Ferrell, 1981). In contrast, recent work in invertebrates has shown that during certain behaviour, such as walking (Graham & Bassler, 1981) and jumping (Steeves & Pearson, 1982), input from joint angle receptors can extensively modify posture and movement. However, other more stereotyped behaviour, such as stridulation (Bassler, 1979) and flight (Wilson, 1961), can be performed in the absence of inputs from joint angle receptors or with this input experimentally disrupted. Despite the advantageous accessibility of invertebrate nervous systems for study at a cellular level (Hoyle & Burrows, 1973), the neuronal mechanisms underlying this implied plasticity of behavioural effects of joint angle receptors have not yet been determined. The present series of investigations, therefore, were undertaken to study a single, identified group of joint angle receptors of the locust hindleg, the metathoracic femoral chordotonal organ. The goals of these investigations are to define the properties of sensory and motor elements of the locust nervous system that determine the functions of this group of receptors and permit flexibility of coupling in behaviour. The locust metathoracic femoral chordotonal organ was first described by Usherwood, Runion & Campbell (1968), who examined the morphology and responses of the organ and identified it as a joint angle receptor. However, a number of basic questions remained as to the responses of the organ. As noted by Burrows & Horridge (1974, p.59): 'No doubt many motorneuron responses to joint motion are due to the chordotonal organ, but inferences about its central action are limited because we lack the following details: (a) whether some or all units are directional in their response, (b) whether the two directions of motion excite the same or different units in different parts of the range, (c) whether vibration at different parts of the range excites different units which could thus signal position although not tonically.' Further, a number of experiments by Bassler (1968), utilizing lesion or disruption of afferent input, have shown that the organ can substantially affect walking and jumping. However, the interpretation of some of these experiments has been confused by a lack of knowledge about the effects of these operations on chordotonal organ output. For example, Bassler (1968) showed that after cutting one of the ligaments of the organ, jumping could not be elicited. Heitler & Burrows (1977) attributed this Insect proprioception 437 effect, not to a discrete function of the chordotonal organ in the jump, but rather to the fact that the locust perceived its joint as fully extended. In contrast, Pearson, Heitler & Steeves (1980) postulated that the chordotonal organ provided inputs that specifically triggered jumping, although the mechanism by which a joint angle receptor could trigger a movement in a joint held immobile by the co-contraction of antagonist muscles was not determined. The first paper in this series, therefore, re-examines the basic morphology and responses of the chordotonal organ, and also studies the responses of individual receptors by intracellular recording. Subsequent papers utilize the information provided by this study to investigate the specific effects of the chordotonal organ upon motoneurones and interneurones. Few previous studies have examined the responses of chordotonal sensilla by intracellular recording (Mendelson, 1963, 1966), owing in part to technical problems. The locust femoral chordotonal organ has proved amenable to such studies. The cellular properties of these receptors may provide insight into the functions of joint angle receptors in behaviour. METHODS Adult male locusts {Schistocerca gregaria), provided by the University of British Columbia and maintained in laboratory cages at 25°C, were used in all experiments. Anatomy Animals (N = 7) were induced to autotomize one metathoracic leg that was pinned out in a Sylgard resin-coated dish, with the femoro-tibial joint angle at 80°. After removing the tarsus, the leg was gently perfused with Karnovsky's fixative for 30 min. The parts of the distal femur and proximal tibia containing the femoral chordotonal organ and its attachments were then cut out, dehydrated and embedded in Spurr's resin. Serial sections (2 fim) were taken either perpendicular or parallel to the long axis of the leg, stained with toluidine blue, and examined by light microscopy. Individual sections were traced through a drawing tube onto acetate sheets and composite overlays were constructed. Physiology Extracellular recordings Intact animals were restrained in wax so that the outer surface of the femur was held in a horizontal plane facing upwards. A small window was cut into the distal femur to expose the main ligament and flexor attachment of the organ and to cut nerves distal to the receptors. Another window was cut 8-10 mm proximal to the organ and multi- unit recordings were taken from the whole nerve 5bl (Campbell, 1961) using hook electrodes. The femoro-tibial joint angle was monitored either by a potentiometer attached to the tibia (Young, 1970) or with a capacitative transducer (Sandeman, 438 S. N. ZILL 1968). Movements of the tibia were generated manually or with a piezoelectric crystal (as described below). All data were stored on tape for subsequent analysis. Intracellular recordings Animals were mounted dorsal side up and the metathoracic legs held in wax so that the inner surface of one femur was in a horizontal plane (Fig. 1). An insect pin, whose ends had been bent into small loops, was glued to the proximal tibia. One of these loops served as a swivel joint when linked to another pin that was attached to the end of a piezoelectric crystal. The crystal generated smooth movements of the tibia when driven by voltages derived from a wave-form generator. Movements were monitored by a photoelectric cell placed close to a flag that was attached to the tibia. To expose the femoral chordotonal organ, a small window was cut in the cuticle of the distal femur. The tibia was then fully extended and a section of the tendon of the extensor tibiae muscle was removed. The joint was then moved to an angle of 45 ° and a Intracellular electrode Femur PE crystal Pin Fig. 1. Diagram of preparation for intracellular recording. A locust is mounted in wax so that one metathoracic leg lies in a horizontal plane with its inner (medial) surface upwards. Changes in tibial position are generated by a piezoelectric crystal (PE crystal) linked to the tibia by a small pin. Displacements are monitored by a photocell placed close to a flag attached to the distal tibia. A small window is cut in the distal femur to expose the femoral chordotonal organ (CO, enlarged for clarity).
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