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Proprioceptive encoding of head position in the black soldier fly, Hermetia illucens (L.) (Stratiomyidae).

Because the eyes of insects cannot be moved independently of the head, information about head posture is essential for stabilizing the visual world or providing information about the direction of gaze. We examined the external anatomy and physiological capabilities of a head posture proprioceptor, the prosternal organ (PO), located at the base of the neck in the black soldier fly, Hermetia illucens (L.) (Family: Stratiomyidae). The PO is sexually isomorphic and is composed of two fused plates of about 130 mechanosensory hairs set in asymmetrical sockets whose orientation varies across the organ. A multi-joint mechanical coupling between the head, neck membrane, and contact sclerites deflects the hairs more or less to increase or decrease their level of excitation. The PO sensory afferents project to the central nervous system (CNS) via a pair of bilateral prosternal nerves (PN) to the fused thoracic ganglia. Simultaneous recording of spiking activity in the PN and videotaping of wind-induced and voluntary head movements around all three axes of head rotation reveal that a few PN afferents are active at rest, but activity increases tonically in response to head deflections. Activity is significantly modulated by change in head angles around the pitch (+/-40 degrees ), yaw (+/-30 degrees ) and roll (more than +/-90 degrees ) axes, although the dynamic range of spiking activity differs for each axis of rotation. Prosternal nerve afferents are bilaterally excited (inhibited) by pitch down (up); excited (inhibited) by head yaw toward the ipsilateral (contralateral) side; excited by roll down toward the ipsilateral side, but little inhibited by roll toward the opposite side. Although bilateral comparison of activity in PN afferents reliably encodes head posture around a given rotational axis, from the point of view of the CNS, the problem of encoding head posture is ill-posed with three axes of rotation and only two streams of afferent information. Furthermore, when the head is rotated around more than one axis simultaneously, mechanical interactions in the neck modify the responses to postural changes around the three rotational axes, which adds further ambiguity to reliable encoding of head posture. The properties of the PO in this relatively basal fly species are compared to those of higher flies and possible mechanisms of disambiguation are discussed.

Action Potentials↗

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.

Action Potentials↗

Plasticity and proprioception in insects. II. Modes of reflex action of the locust metathoracic femoral chordotonal organ.

Reflex responses of tibial motoneurones were examined during mechanical stimulation of the femoral chordotonal organ, a joint angle receptor of the locust hindleg. Step displacements of the main ligament of the organ, mimicking 10-15 degree changes in joint angle, produced different patterns of discharge in motoneurones (1) when the leg was resting against a support and (2) when the support was removed to induce active searching movements. Tibial motoneurones showed resistance reflex responses to oppose the apparent joint movement when the leg rested against a support. Resistance reflexes consisted of constant, short latency excitatory responses followed by discharges that varied in intensity (gain) and degree of tonic coupling. These variations were not due to simple summation with other inputs to motoneurones. Responses changed during periods of active searching movements. Tibial flexor motoneurones fired phasically in response to apparent joint movement in any direction. Tibial extensor motoneurones were generally inhibited by chordotonal inputs. These reflex changes are not simple reflex 'reversals', but represent more complex changes in reflex mode. Potential functions of each of these reflex modes and the need for plasticity in reflexes of the chordotonal organ are discussed.

Animals↗

Connections between thoraco-coxal proprioceptive afferents and motor neurons in the locust.

The position of the coxal segment of the locust hind leg relative to the thorax is monitored by a variety of proprioceptors, including three chordotonal organs and a myochordotonal organ. The sensory neurons of two of these proprioceptors, the posterior joint chordotonal organ (pjCO) and the myochordotonal organ (MCO), have axons in the purely sensory metathoracic nerve 2C (N2C). The connections made by these afferents with metathoracic motor neurons innervating thoraco-coxal and wing muscles were investigated by electrical stimulation of N2C and by matching postsynaptic potentials in motor neurons with afferent spikes in N2C. Stretch applied to the anterior rotator muscle of the coxa (M121), with which the MCO is associated, evoked sensory spikes in N2C. Some of the MCO afferent neurons make direct excitatory chemical synaptic connections with motor neurons innervating the thoraco-coxal muscles M121, M126 and M125. Parallel polysynaptic pathways via unidentified interneurons also exist between MCO afferents and these motor neurons. Connections with the common inhibitor 1 neuron and motor neurons innervating the thoraco-coxal muscles M123/4 and wing muscles M113 and M127 are polysynaptic. Afferents of the pjCO also make polysynaptic connections with motor neurons innervating thoraco-coxal and wing muscles, but no evidence for monosynaptic pathways was found.

Afferent Pathways↗

Proprioception at the ankle: the effect of anaesthetic blockade of ligament receptors.

Seven subjects with normal joints were tested for active and passive position sense of ankle inversion, peroneal reflex reaction time to sudden ankle inversion, and postural stability during single-leg stance. The tests were performed before and after regional block of the ankle and foot with local anaesthetic. Passive position sense, assessed with the muscles relaxed, was greatly impaired by anaesthesia but active position sense, with the calf muscles activated, was preserved, and the peroneal reaction time to sudden ankle inversion was not altered. The magnitude of postural sway during single-leg stance was also unchanged by anaesthesia of the ankle and foot. The results suggest that the afferent input from intact lateral ankle ligaments is important in sensing correct placement of the foot at heel-strike, but that this input can be replaced by afferent information from active calf muscles. Afferent input from these muscles seems also to be responsible for dynamic ankle protection against sudden ankle inversion and is adequate to allow stable single-leg stance.

Adult↗

Proprioceptive accuracy in two dimensions.

Slow arm movements were made over a smooth horizontal table at shoulder height. With visual cues excluded, target position was indicated by the index finger of the nonmoving arm touching the underside of the table. 11 students (mean age 21.9 yr.) and 24 children (mean age 10.3 yr.) were compared. Both groups showed an 'overlap effect': movements with the right hand went too far to the left, while movements with the left hand went too far to the right. The children as a group were significantly less accurate than the students and showed a significant asymmetry in that movements with the dominant hand were more accurate than those with the nondominant hand.

Adult↗

Matching proprioceptive to visual speed affected by nonkinematic parameters.

In an experiment three subjects adjusted the speed of a treadmill under their feet to match the speed of a flow pattern visible in front of their feet. Although the subjects could perform the matching fairly well, their adjustment varied with the effort of walking manipulated. This finding rules out a purely kinematic-matching hypothesis.

Acceleration↗

Proprioceptive training for learning downhill skiing.

The aim was to assess whether balance training would improve downhill skiing for 30 physical education students who had no previous skiing experience and were randomly assigned to two groups. The control group attended only ski lessons for two weeks, 2 to 4 hours daily. The experimental group attended downhill ski lessons and indoor balance training on a balance board, wearing ski boots, for 20 min. every second day in the afternoon. All participants before training completed a balance assessment (stability indices). After the completion of the ski classes, all repeated the balance assessment and two downhill ski tests of agility, slalom and snow-ploughing techniques. Analysis of variance with repeated measures showed both groups improved balance similarly, but the experimental group performed significantly better on the downhill-slalom agility test, so the specific indoor balance training was helpful.

Adult↗

Foot and ankle sensory neuropathy, proprioception, and postural stability.

Foot and ankle sensory neuropathy may result from a variety of pathologic conditions, especially diabetes mellitus. Decreased sensation, particularly on the plantar surface of the feet, leads to obvious risks of cutaneous injury. Less obvious are the risks of fall-related injury associated with changes in other sensory systems of the foot and ankle, such as the receptors involved in joint movement and position perception. The results of a number of studies demonstrate that the neuropathic process affects these receptors in individuals with diabetes mellitus. Associated with the decreased sensory function of the foot and ankle is decreased performance on tests of static and dynamic postural stability. Subjective feelings of instability and an increased incidence of fall-related injuries have also been reported. The reduced postural stability in persons with diabetic neuropathy cannot be attributed exclusively to loss of plantar cutaneous sensation; it appears to be the result of a general loss of peripheral sensory receptor function in the lower legs, including that of the muscle spindles. During the evaluation of an individual with foot and ankle sensory neuropathy, the possibility of balance deficits should be given proper attention. Assessment of balance deficits could be particularly important when planning the course of rehabilitation for individuals with foot and ankle neuropathy who use modified footwear or have an amputation of a section of the foot or lower extremity.

Ankle↗

Otolithic and extraocular muscle proprioceptive influences on the spatial organization of the vestibulo- and cervico-ocular quick phases.

The cervico-ocular reflex (COR) was studied alone or in combination with the vestibulo-ocular reflex (VOR) in the rabbit. Step stimulations of the body with respect to the fixed head induced small slow compensatory responses followed by large compensatory quick phases (QP). These responses remained aligned with the horizon at different head pitch angles. The QP reorientation in space was due to the gravity influence on the otolithic receptors. The vestibular induced QPs exhibit a similar pattern. Because of this reorientation, the reduction of the amplitude of the vestibular induced QPs, due to the addition of the COR, was maintained even at different static head positions. The electrolytic lesion of the ophthalmic branch of the trigeminal nerve deeply affected the space orientation of the COR. In particular, the cervically induced compensatory QPs of the eye ipsilateral to the lesion showed a remarkable variability of their trajectories and they lost space reorientation. These findings suggest that the coordinate system controlling the QPs is influenced by signals originating from both head position in space and eye position in the orbit.

Animals↗