Gravity reception in the walking fly, Calliphora erythrocephala: Tonic and modulatory influences of leg afferents on the head position

The proprioceptive gravity receptor system of the fly, Calliphora erythrocephala, is functionally organized in a manner similar to the statocyst system in vertebrates, molluscs and crustaceans. It includes one system in which excitation is modulated by the gravitational stimulus, and another which exerts a tonic excitation on the neurones of the reflex arc between the leg receptors and the neck muscles. While the modulating system for the compensatory head movement of the walking flies is located only in the forelegs and the middle legs, the tonic excitation is mediated by receptors of all legs.     

Mutual influences of upper and lower extremities during cyclic movements

The possibility for the activation of muscles in a passive arm during its cyclic movements imposed by active movements of the contralateral arm or by an experimenter and the effect that the movements of lower extremities have on the activity of the arm muscles have been studied. In addition, the activity of the leg muscles was studied as dependent on the motor task performed by the arms. Ten healthy subjects performed antiphase arm movements with and without stepping-like movements of both legs in the supine position. The experiment was performed under three conditions for the arm movements: (1) both arms performed active movements; (2) one arm performed active movements, and the contralateral arm, being entirely passive, was forced to participate in movements; (3) the movement of the passive arm was caused by an experimenter. Under condition (2), additional loadings of 30 and 60 N were applied to the active arm. Under all conditions, the arm movements were performed with and without leg movements. The possibility for the activation of muscles in the arm performing passive movements has been demonstrated. To a large extent, this is possible due to an increase in the afferent inflow from the muscles of the contralateral arm. The electrical activity was modulated during cyclic arm movements and depended on the level of loading of the active arm. During the combined active movements of the arms and legs, the reduction in the activity of the flexor muscles of the shoulder and forearm was observed. In the case of passive stepping-like movements, the concomitant arm movements increased the magnitude of electromyographic bursts in most of the examined leg muscles. During active leg movements, a similar increase in electromyographic bursts was observed only in the m. biceps femoris (BF) and the anterior tibial muscle. An increase in the loading of one arm caused a significant increase in the EMG activity in most examined muscles of the legs. The data obtained provide additional proof for the existence of a functionally significant neuronal interaction between the arms, as well as between the upper and lower extremities, which is probably due to intraspinal neuronal connections.     

On the invariance of visual stimulus efficacy with respect to variable spatial positions

Summary In the fly,Calliphora erythrocephala, visual stimuli presented in an asymmetrical position with respect to the fly elicit roll or tilt movements of the head by which its dorsal part is moved towards the light areas of the surroundings (Figs. 4–7). The influence of passive body roll and tilt (gravitational stimulus) on the amplitude of these active head movements was investigated for two types of visual stimuli: (1) a dark hollow hemisphere presented in different parts of the fly's visual field, and (2) a moving striped pattern stimulating the lateral parts of one eye only.The response characteristics of the flies in the bimodal situation in which the gravitational stimulus was paired with stimulation by the dark hollow hemisphere can be completely described by the addition of the response characteristics for both unimodal situations, i.e. by the gravity-induced and visually induced characteristics (Figs. 8, 9). Therefore, the stimulus efficacy of the dark hollow hemisphere is independent of (=invariant with respect to) the flies' spatial position. The advantage of this type of interaction between gravity and visual stimulation for the control of body posture near the horizontal is discussed.In contrast, the efficacy of moving patterns depends on (=non-invariant with respect to) the spatial position of the walking fly. Regressive pattern movements exhibit their stronger efficacy with respect to progressive ones only when the gravity receptor system of the legs is stimulated. The stronger efficacy of downward vs upward movements can only be demonstrated when the flies are walking horizontally, independently of whether the leg gravity receptor system is stimulated by gravity or not (Fig. 10).The results are discussed with respect (1) to the invariance and non-invariance of the efficacy of visual stimuli with respect to the direction of the field of gravity, (2) to the formation of reference lines by the gravitational field which are used by the walking fly to determine the orientation of visual patterns, and (3) to the possible location of the underlying convergence between gravitationally and visually evoked excitation. As all types of head responses occur only in walking flies, we also discussed the possible influences of some physiological processes like arousal, proprioceptive feedback during walking and various peripheral sensory inputs on the performance of behavioural responses in the fly (Fig. 11).     

Steering responses of adult and nymphal crickets to light,with special reference to the head rolling movement

Most tethered adult crickets (Gryllus bimaculatus) assumed flight postures with or without flapping their wings in a windstream. Nymphal crickets (sixth and seventh, i.e. final, instars) also displayed the flight posture in spite of the incompleteness of wing development. These adult nymphal crickets rolled their heads towards the light source in response to unequal illumination of the compound eyes only while maintaining the flight posture. The amphtude of the head rolling movements was proportional to the change of light position up to 120°C, and independent of the light intensity if the duration was longer than 1 sec. The unequal illumination could also induce a transient increase in discharge frequency of the wing muscles on both sides, a decrease in wing beat amplitude of the ipsilateral wing on the illuminated side, and bending movements of the legs and abdomen towards the light. Cutting either of the nerve connectives at any level between the subosophageal and metathoracic ganglia did not affect the response of either the head or the abdomen to illumination. These results are discussed in relation to the steering mechanism associated with the dorsal light reaction.     

Low-frequency airborne vibrations generated by crickets during singing and aggression

When crickets (Gryllus bimaculatus) produce their calling, courtship and rivalry songs, they generate, in addition to the audible stridulatory sound, low-frequency air oscillations associated with the inward and outward movements of the forewings. The frequencies of these oscillations are below ca 70 Hz, with a major component at 30 Hz, the syllable repetition rate. In the courtship song, single oscillations are also produced. Jerking movements of the whole body, which often occur in the presence of rivals, cause considerable air currents. In all these cases the air vibrations are sufficient to be perceived both by the individual generating them and by conspecifics (and perhaps by other insects) via air-flow receptors, in crickets the cercal filiform hairs.     

Activation of interlimb interactions increases the motor output in legs of healthy subjects: Study under the conditions of arm and leg unloading

The effect of arm movements and movements of individual arm joints on the electrophysiological and kinematic characteristics of voluntary and vibration-triggered stepping-like leg movements was studied under the conditions of horizontal support of the upper and lower limbs. The horizontal support of arms provided a significant increase in the rate of activation of locomotor automatism by noninvasive impact on tonic sensory inputs. The addition of active arm movements during involuntary stepping-like leg movements led to an increase in the EMG activity of hip muscles and was accompanied by an increase in the amplitude of hip and shin movements. The movement of the shoulder joints led to an increase in the activity of hip muscles and was accompanied by an increase in the amplitude of hip and shin movements. Passive arm movements had the same effect on induced leg movements. The movement of the shoulder joints led to an increase in the activity of hip muscles and an increase in the amplitude of movements of knee and hip joints. At the same time, the movement of forearms and wrists had a similar facilitating effect on the physiological and kinematic characteristics of rhythmic stepping-like movements, but influenced the distal segments of legs to a greater extent. Under the conditions of subthreshold vibration of leg muscles, voluntary arm movements led to activation of involuntary rhythmic stepping movements. During voluntary leg movements, the addition of arm movements had a significantly smaller impact on the parameters of rhythmic stepping than during involuntary leg movements. Thus, the simultaneous movements of the upper and lower limbs are an effective method of activation of neural networks connecting the rhythm generators of arms and legs. Under the conditions of arm and leg unloading, the interactions between the cervical and lumbosacral segments of the spinal cord seem to play the major role in the impact of arm movements on the patterns of leg movements. The described methods of activation of interlimb interactions can be used in the rehabilitation of post-stroke patients and patients with spinal cord injuries, Parkinson’s disease, and other neurological diseases.     

Mutual influences of upper and lower extrimities during cyclic movements

The possibility of muscle activation of passive arm during its cyclic movements, imposed by active movements of contralateral arm or by experimenter was studied, as well as the influence of lower extremities cyclic movements onto arm muscles activity. In addition to that the activity of legs muscles was estimated in dependence on motor task condition for arms. Ten healthy supine subjects carried out opposite movements of arms with and without stepping-like movements of both legs. The experiment included three conditions for arm movements: 1) the active movements of both arms; 2) the active movements of one arm, when other entirely passive arm participated in the movement by force; 3) passive arm movement caused by experimenter. In the condition 2) additional load on active arm was applied (30 N and 60 N). In all three conditions the experiment was carried out with arms movements only or together with legs movements. The capability of passive moving arm muscles activation depended on increasing afferent inflow from muscles of contralateral arm was demonstrated. Emerging electrical activity was modulated in the arms movements cycle and depended on the degree of active arm loading. During combined active movements of arms and legs the reduction of activity in the flexor muscles of shoulder and forearm was observed. Concomitant arms movements increased the magnitude ofelectromiographic bursts during passive stepping-like movements in the most of recorded muscles, and the same increasing was only observed in biceps femoris and tibialis anterior muscles during active legs movement. The increasing of loading of one arm caused essential augmentation of EMG-activity in the majority of recording legs muscles. The data obtained are the additional proof of existence of functionally significant neuronal interaction both between arms and between upper and lower extremities, which is evidently depend on the intraspinal neuronal connections.     

Method to Measure Tone of Axial and Proximal Muscle

The control of tonic muscular activity remains poorly understood. While abnormal tone is commonly assessed clinically by measuring the passive resistance of relaxed limbs¹, no systems are available to study tonic muscle control in a natural, active state of antigravity support. We have developed a device (Twister) to study tonic regulation of axial and proximal muscles during active postural maintenance (i.e. postural tone). Twister rotates axial body regions relative to each other about the vertical axis during stance, so as to twist the neck, trunk or hip regions. This twisting imposes length changes on axial muscles without changing the body''s relationship to gravity. Because Twister does not provide postural support, tone must be regulated to counteract gravitational torques. We quantify this tonic regulation by the restive torque to twisting, which reflects the state of all muscles undergoing length changes, as well as by electromyography of relevant muscles. Because tone is characterized by long-lasting low-level muscle activity, tonic control is studied with slow movements that produce "tonic" changes in muscle length, without evoking fast "phasic" responses. Twister can be reconfigured to study various aspects of muscle tone, such as co-contraction, tonic modulation to postural changes, tonic interactions across body segments, as well as perceptual thresholds to slow axial rotation. Twister can also be used to provide a quantitative measurement of the effects of disease on axial and proximal postural tone and assess the efficacy of intervention.     

The function of auditory neurons in cricket phonotaxis

Summary The activity of auditory receptor cells and prothoracic auditory neurons of the cricket,Gryllus bimaculatus, was recorded intracellularly while the animal walked on a sphere or while passive movement was imposed on a foreleg.During walking the responses to simulated calling song is altered since (i) the auditory sensory cells and interneurons discharged impulses in the absence of sound stimuli (Figs. 1, 3) and (ii) the number of action potentials in response to sound is reduced in interneurons (Figs. 2, 3).These two effects occurred in different phases of the leg movement during walking and therefore masked, suppressed or did not affect the responses to auditory stimuli (Figs. 3, 4). Hence there is a time window within which the calling song can be detected during walking (Fig. 5).The extra excitation of receptors and interneurons is probably produced by vibration of the tympanum because (i) the excitation occurred at the same time as the leg placement (Fig. 4), (ii) during walking on only middle and hindlegs, no extra action potentials were observed (Fig. 6), (iii) in certain phases of passive movements receptor cells and interneurons were excited as long as the ipsilateral ear was not blocked (Figs. 8, 9).Suppression of auditory responses seems to be peripheral as well as central in origin because (i) it occurred at particular phases during active and passive leg movements in receptor cells and interneurons (Figs. 1, 4, 9), (ii) it disappeared if the ear was blocked during passive leg movements (Fig. 9) and (iii) it persisted if the animal walked only on the middle and hind legs (Fig. 6).     

The influence of substrate contact on gravity orientation

Summary Tilting of the animal with respect to gravity results in compensatory eyestalk movements and in leg counterforce reactions which vary with the number and sequential position of legs touching the body-fixed substrate board (Figs. 2, 3). The gravity response is reduced with increasing number of legs touching the substrate. The results fit an interpretation that the weight of the substrate input interacting with gravity signals results from superposition of the weighted effects of the single legs involved (Figs. 2, 4).Acknowledgements are due to the Max-Planck-Institut (D. M. Neil, N. Scapini) and to the Carnegie Trust (D. M. Neil) for financial support. We want to thank renate Alton for her co-operative help.     

Rearing under different conditions results in different functional recoveries of giant interneurons in unilaterally cercus-ablated crickets, Gryllus bimaculatus

The effects of rearing conditions on the functional recovery of wind-sensitive giant interneurons (GIs) after unilateral cercal ablation were investigated in the cricket, Gryllus bimaculatus. Crickets were reared in a glass vials to prohibit free walking for 14 days after unilateral cercal ablation ("14-day vial" crickets). Other crickets were reared in an apparatus called a "walking inducer" (WI) to increase the walking distance during the same 14-day period ("14-day WI" crickets). In these crickets, the response properties of GIs 8-1, 9-1, 9-2, and 9-3 to air currents from various directions were investigated. From the intensity-response curves obtained, directionality curves expressed in terms of threshold velocity and response magnitude were made independently. To understand changes in the functional recovery of GIs more thoroughly, the directional characteristics of GIs in crickets 1 day after unilateral cercal ablation ("1-day free" crickets) were also compared. Between the 1-day free and 14-day vial crickets, all the GIs showed differences in both threshold velocity and response magnitude for some stimulus directions. Between the 14-day vial and 14-day WI crickets, differences in the threshold velocities of GIs 9-1, 9-2, and 9-3, and in the response magnitudes of GIs 8-1, 9-1, and 9-3 were detected. Because the rearing condition after unilateral cercal ablation largely affects the compensatory recovery in some parameters of wind-evoked escape behavior, such as relative occurrence and escape direction, we discuss the functional differences in GIs revealed here in relation to the roles of GIs in the neural system that controls escape behavior.     

The control of antennal movements by leg proprioceptors in the rock lobster,Palinurus vulgaris

Summary The antennae of the rock lobster,Palinurus vulgaris, show systematic responses to movements of the legs on a tilting footboard. Myographic recordings in muscles of the first antennal segment have been used in an analysis of the sensory basis of these reactions. Antennal posture is modified in the experimental apparatus, although its relation to the change in loading conditions of the legs is uncertain. The motor control of the antennal equilibrium responses involves a complete reciprocation between both excitatory and inhibitory motoneurones to the antagonist muscle groups in the two antennae. Sensory inputs from single legs produce movements of both antennae, but a stronger drive ipsilaterally. Leg receptor inputs also modulate antennal resistance reflexes in a systematic manner, providing a sensitive test for the involvement of particular receptor organs in the leg. Movement at the coxo-basal leg joint is a major source of sensory input, and ablation/ stimulation experiments have established that stimulation of the CB chordotonal organ is a necessary but not sufficient condition to produce the antennal equilibrium reactions. The possibility is discussed that other receptors at the coxo-basal joint are also involved.D.M.N. was supported by a grant from The Max-Planck Institut to Professor H. Schöne.     

Interlimb interactions during cyclic in-phase and antiphase movements of arms and legs and their dependence on afferent influences

Coordinated arm and leg movements imply neural interactions between the rhythmic generators of the upper and lower extremities. In ten healthy subjects in the lying position, activity of the muscles of the upper and lower extremities was recorded during separate and joint cyclic movements of the arms and legs with different phase relationships between the movements of the limbs and under various conditions of the motor task. Antiphase active arm movements were characterized by higher muscle activity than during the inphase mode. The muscle activity during passive arm movements imposed by the experimentalist was significantly lower than muscle activity during passive arm movements imposed by the other arm. When loading one arm, the muscle activity in the other, passively moving, arm increased independently from the synergy of arm movements. During a motor task implementing joint antiphase movements of both upper and lower extremities, compared to a motor task implementing their joint in-phase movements, we observed a significant increase in activity in the biceps brahii muscle, the tibialis anterior muscle, and the biceps femoris muscle. Loading of arms in these motor tasks has been accompanied by increased activity in some leg muscles. An increase in the frequency of rhythmic movements resulted in a significant growth of the muscle activity of the arms and legs during their cooperative movements with a greater rate of rise in the flexor muscle activity of the arms and legs during joint antiphase movements. Thus, both the spatial organization of movements and the type of afferent influences are significant factors of interlimb interactions, which, in turn, determine the type of neural interconnections that are involved in movement regulation.     

Activity of neck-muscle motoneurones during eye cleaning behaviour in the cricket Gryllus campestris

The activity of neck-muscle motoneurones which control head movements during eye cleaning behaviour was recorded from motor nerves with chronically implanted electrodes in unrestrained crickets. We show that motoneurones of the dorso-ventral muscles displayed strong activity differences between both sides of the neck, with higher discharge frequencies either ipsi- or contralateral to the direction of the head movement. Motoneurones innervating dorsal-longitudinal muscles were equally active on both sides. A single excitatory motoneurone of one dorso-ventral muscle showed a discharge pattern unequivocally related to eye cleaning. Lesions of connectives revealed that this motoneurone is monitored by interneuronal pathways from the suboesophageal ganglion although the primary sensory axons eliciting eye cleaning, project into the prothoracic ganglion.     

Neuronal mechanisms of motor signal transmission in the thalamic ventrooral nucleus in spasmodic torticollis patients

A microelectrode technique was used to study the neuronal mechanisms of motor signal transmission in the ventrooral internus nucleus (Voi) of the motor thalamus during voluntary and involuntary pathological (dystonic) movements in patients with spasmodic torticollis. Voi cell elements proved highly reactive to various functional (mostly motor) tests. An activity analysis of 55 Voi neurons detected during nine stereotactic operations revealed, first, a difference in neuronal mechanisms of motor signal transmission for voluntary movements that do or do not involve the affected axial muscles of the neck and for passive and abnormal involuntary dystonic movements. Second, a sensory component was found to play a key role in the mechanisms of sensorimotor interactions during voluntary and involuntary dystonic head and neck movements activating the axial muscles of the neck. Third, rhythmic and synchronized activity of Voi neurons was shown to play an important role in motor signal transmission during voluntary and passive movements. The Voi nucleus was directly implicated in the mechanisms of involuntary head movements and tension of the neck muscles in spasmodic torticollis. The results can be used to identify the Voi nucleus of the thalamus during stereotactic neurosurgery in order to select the optimal destruction or stimulation target and to reduce the postoperative effects in spasmodic torticollis patients.     

The influence of initial posture on the sit-to-stand movement

Head movements, ground reaction forces and electromyographic activity of selected muscles were recorded simultaneously from two subjects as they performed the sit-to-stand manouevre under a variety of conditions. The influence of initial leg posture on the magnitude of the various parameters under investigation was examined first. A preferred initial leg posture resulted in smaller magnitudes of head movement and ground reaction forces. EMG activity in some muscles, trapezius and erector spinae, decreased, while in others, quadriceps and hamstrings, it increased in the preferred leg posture. The decreases seen correlate with reductions in head movement observed. The effect of inhibiting habitual postural adjustments of the head and neck, by comparing "free" and "guided" movements was also examined. In guided movements there are significant reductions in head movement, ground reaction forces and EMG activity in trapezius, sternomastoid and erector spinae. It would appear that both initial leg posture and the abolition of habitual postural adjustment have a profound influence on the efficiency of the sit-to-stand manouevre. This preliminary study high-lights the practical importance of head posture in the diagnosis and treatment of movement disorders, as well as in movement education.     

Are interlimb interactions disturbed in patients with Parkinson’s disease? A study under unloading conditions

During natural human locomotion, neural connections are activated that are typical of regulation of the quadrupedal walking. The interaction between the neural networks generating rhythmic movements of the upper and lower limbs depends on tonic state of each of these networks regulated by motor signals from the brain. Distortion of these signals in patients with Parkinson’s disease (PD) may lead to disruption of the interlimb interactions. We examined the effect of movements of the limbs of one girdle on the parameters of the motor activity of another limb girdle at their joint cyclic movements under the conditions of arm and leg unloading in 17 patients with PD and 16 healthy subjects. We have shown that, in patients, the effect of voluntary and passive movements of arms, as well as the active movement of the distal parts of arms, on the voluntary movement of legs is weak, while in healthy subjects, the effect of arm movements on the parameters of voluntary stepping is significant. The effect of arm movements on the activation of the involuntary stepping by vibrational stimulation of-legs in patients was absent, while in healthy subjects, the motor activity of arms increased the possibility of involuntary rhythmic movements activation. Differences in the effect of leg movements on the rhythmic movements of arms were found in both patients and healthy subjects. The interlimb interaction appeared after drug administration. However, the effect of the drug was not sufficient for the recovery of normal state of the neural networks in patients. In PD patients, neural networks generating stepping rhythm have an increased tonic activity, which prevents the activation and appearance of involuntary rhythmic movements facilitating the effects of arms on legs.     

The investigation of control mechanisms of stepping rhythm in human in the air-stepping conditions during passive and voluntary leg movements

In unloading condition the degree of activation of the central stepping program was investigated during passive leg movements in healthy subjects, as well as the excitability of spinal motoneurons during passive and voluntary stepping movement. Passive stepping movements with characteristics maximally approximated to those during voluntary stepping were accomplished by experimenter. The comparison of the muscle activity bursts during voluntary and imposed movements was made. In addition to that the influence of artificially created loading onto the foot to the leg movement characteristics was analyzed. Spinal motoneuron excitability was estimated by means of evaluation of amplitude modulation of the soleus H-reflex. The changes of H-reflexes under the fixation of knee or hip joints were also studied. In majority of subjects the passive movements were accompanied by bursts of EMG activity of hip muscles (and sometimes of knee muscles), which timing during step cycle was coincided with burst timing of voluntary step cycle. In many cases the bursts of EMG activity during passive movements exceeded activity in homonymous muscles during voluntary stepping. The foot loading imitation exerted essential influence on distal parts of moving extremity during voluntary as well passive movements, that was expressed in the appearance of movements in the ankle joint and accompanied by emergence and increasing of phasic EMG activity of shank muscles. The excitability of motoneurons during passive movements was greater then during voluntary ones. The changes and modulation of H-reflex throughout the step cycle without restriction of joint mobility and during exclusion of hip joint mobility were similar. The knee joint fixation exerted the greater influence. It is supposed that imposed movements activate the same mechanisms of rhythm generation as a supraspinal commands during voluntary movements. In the conditions of passive movements the presynaptic inhibition depend on afferent influences from moving leg in the most degree then on central commands. It seems that afferent inputs from pressure receptors of foot in the condition of "air-stepping" actively interact with central program of stepping and, irrespective of type of the performing movements (voluntary or passive), form the final pattern activity.     

The investigation of locomotor activity control system in humans under the air-stepping conditions during passive and voluntary leg movements

The degree of activation of the central stepping program during passive leg movement was studied in healthy subjects under unloading conditions; the excitability of spinal motoneurons was studied during passive and voluntary stepping movements. Passive stepping movements with characteristics maximally close to those during voluntary stepping were accomplished by the experimenter. The bursts of muscular activity during voluntary and imposed stepping movements were compared. In addition, the influence on the leg movement of artificially created loading onto the foot was studied. The excitability of spinal motoneurons was estimated by the amplitude of modulation of the m. soleus H reflex. Changes in the H reflex (Hoffmann’s reflex) after fixation of the knee and hip joints were also studied. In most subjects, passive movements were accompanied by bursts of electromyographic (EMG) activity in the hip muscles (sometimes in shank muscles); the timing of the EMG burst during the step cycle coincided with the burst’s timing during voluntary stepping. In many cases, the bursts in EMG activity exceeded the activity of homonymous muscles during voluntary stepping. Simulation of foot loading influenced significantly the distal part of the moving extremity during both voluntary and passive movements, which was expressed in the appearance of movements in the ankle joint and an increase in the phasic EMG activity of the shank muscles. The excitability of motoneurons during passive movements was higher than during voluntary movements. Changes and modulation of the H reflex throughout the step cycle were similar without restriction of joint mobility and without hip joint mobility. Fixation of the knee joint was of great importance. It is supposed that imposed movements activate the same mechanisms of rhythm generation as supraspinal commands during voluntary movements. During passive movements, presynaptic inhibition depends mostly on the afferent influences from the moving leg rather than on the central commands. Under the conditions of “air-stepping,” the afferent influences from the foot pressure receptors are likely to interact actively with the central program of stepping and to determine the final activity pattern irrespective of the movement type (voluntary or passive).