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Role of presynaptic inputs to proprioceptive afferents in tuning sensorimotor pathways of an insect joint control network.

The femur-tibia (FT) joint of insects is governed by a neuronal network that controls activity in tibial motoneurons by processing sensory information about tibial position and movement provided by afferents of the femoral chordotonal organ (fCO). We show that central arborizations of fCO afferents receive presynaptic depolarizing synaptic inputs. With an average resting potential of -71.9 +/- 3.72 mV (n = 10), the reversal potential of these potentials is on average -62.8 +/- 2.3 mV (n = 5). These synaptic potentials occur either spontaneously or are related to movements at the fCO. They are thus induced by signals from other fCO afferents. Therefore, the synaptic inputs to fCO afferents are specific and depend on the sensitivity of the individual afferent affected. These potentials reduce the amplitude of concurrent afferent action potentials. Bath application of picrotoxin, a noncompetitive blocker of chloride ion channels, blocks these potentials, which indicates that they are mediated by chloride ions. From these results, it is concluded that these are inhibitory synaptic potentials generated in the central terminals of fCO afferents. Pharmacologic removal of these potentials affects the tuning of the complete FT control system. Following removal, the dependence of the FT control loop on the tibia position increases relative to the dependency on the velocity of tibia movements. This is due to changes in the relative weighting of the position and velocity signals in the parallel interneuronal pathways from the fCO onto tibial motoneurons. Consequently, the FT joint is no longer able to perform twig mimesis (i.e., catalepsy), which is known to rely on a low position compared to the high-velocity dependency of the FT control system.

Afferent Pathways↗

Normal proprioceptive trigeminal afferents in patients with Sjögren's syndrome and sensory neuronopathy.

A pure sensory neuropathy due to neuronal damage in the gasserian and spinal ganglia has been described in patients with Sjögren's syndrome. Conventional electromyographic (EMG) studies can demonstrate the selective involvement of the sensory pathways but they do not provide definite evidence for the site of the lesion. Noting that the trigeminal sensory neurons carrying cutaneous and muscular afferents are differentially located in the gasserian and mesencephalic nuclei, respectively, we carried out an electrophysiological study of the trigeminofacial and trigeminotrigeminal reflexes in 5 patients with Sjögren's syndrome and pure sensory neuropathy, in 10 patients with sensory-motor neuropathies of other causes, and in 10 healthy subjects. Our results show that patients with Sjögren's syndrome and pure sensory neuropathy who exhibited abnormal blink reflexes and an abnormal, cutaneous-induced masseter silent period had normal jaw jerks, whereas patients with sensory-motor neuropathies who exhibited abnormal cutaneous responses had abnormal jaw jerks. These findings suggest that the lesion in pure sensory neuropathy involves damage to the neurons of the gasserian ganglia and not to the trigeminal axons, since an axonal lesion would be expected to involve the large axons from muscle spindle receptors.

Adult↗

Reactions of the geniculate cells to extraocular proprioceptive activation in rabbits.

The aim of these investigations was to advance our knowledge of the influence of extrinsic ocular muscle (EOM) stretching on cell excitability of the retinocortical pathway. The initial goal was the lateral geniculate; however, histologic analysis indicated that most cells that responded to stretching were located near its superior edge, in an area analogous to the perigeniculate. Rabbits were anaesthetized and prepared for single-cell recordings. The extraocular muscles were detached from the eye and attached to a rigid tungsten hook. The hook was soldered to the pivot of a galvanometer that was controlled by a waveform generator. Precise and repeated length changes were obtained with extension and relaxation ramps of constant velocity. Thirty percent of the units (N = 250) responded to EOM stretching. These stimuli evoked either an excitation or a decrease of the units' spontaneous activity. Several experimental controls provided evidence that the signals that evoked the geniculate responses originated from proprioceptors belonging to the EOM. Most responding cells had their receptive fields located eccentrically (greater than or equal to 50 degrees). Also, cells that reacted to EOM stretching responded to optic nerve stimulation with a significantly shorter latency than cells that were unresponsive. Pairing the EOM stretching with light stimuli produced the following results. In about half of the units the light-evoked responses augmented, but in 28% of the cells the light-evoked discharges decreased. These effects were obtained even though EOM stretching delivered singly failed to elicit a reaction from the cell. Histologic reconstructions indicated that cells were distributed in a discrete region lying rostral and dorsomedial to the lateral geniculate nucleus. This area has been associated with the perigeniculate nucleus in cats and rats.

Animals↗

What is the role of muscle receptors in proprioception?

The role of muscle afferents is discussed in terms of their contribution to kinesthesia, the senses of position and movement of the limbs. It is argued that muscle spindles are not well suited as position sensors, on several grounds. Yet we know from muscle vibration experiments that they do contribute to kinesthesia. A number of recent experiments have shown that positional information is of particular significance to the central nervous system. In other experiments it has been demonstrated that a disturbance to kinesthesia follows fatigue from exercise. Fatigue of elbow flexor muscles led subjects to make significant positional errors in a forearm matching task. The size of the errors correlated with the fall in force from fatigue. These data suggest that we derive a positional cue from the effort required to hold a limb against the force of gravity. A challenge for the future will be to reveal how the centrally derived sense of effort and peripherally derived afferent information interact to give us our kinesthetic sense.

Animals↗

Octopamine effects mimick state-dependent changes in a proprioceptive feedback system.

The modulatory actions of the biogenic amine octopamine on the femur tibia (FT) control loop in the stick insect Carausius morosus were examined. The response properties of the FT control loop were determined under open loop conditions. Mechanical stimulation of the femoral chordotonal organ (fCO) was the input and tibial movement and motoneuronal activity were measured as the output of the system. Following octopamine injection into the hemolymph of intact, inactive animals, two consecutive phases occurred at the behavioral level. Octopamine caused initially an activation of the animal. During this first phase (3.5-12 min duration) the response properties of the FT control loop were similar to those found in animals that were activated by tactile stimuli under normal conditions. Afterward, animals became inactive. During this second phase (15-20 min duration), the gain of the control loop was zero and no resistance reflex in the FT joint was generated in response to fCO stimulation. However, active movements of the tibia could still be elicited. As we could show in restrained animals, where DL-octopamine was applied topically onto the undesheated mesothoracic ganglion, the complete suppression of the resistance reflex on the motoneuronal level was dose dependent starting at concentrations of 5 x 10(-3) M octopamine. We could show that octopamine specifically suppressed the pathways involved in the resistance reflex, while feedback loop responses to fCO stimuli typical for active animals could still be elicited. Our results indicate that an increase in the octopamine concentration mimicks activation of the animal: Properties being characteristic for the control of the FT joint in the inactive animal are inhibited by octopamine, while properties of the FT control loop typical for the active animal appear to be facilitated following octopamine injection. The results clearly demonstrate that different pathways in the neuronal network underlying the FT control loop are involved in the responses of the control loop to fCO stimuli in the inactive and active behavioral states of the stick insect.

Animals↗

Adaptation to Coriolis force perturbation of movement trajectory; role of proprioceptive and cutaneous somatosensory feedback.

Subjects exposed to constant velocity rotation in a large fully-enclosed room that rotates initially make large reaching errors in pointing to targets. The paths and endpoints of their reaches are deviated in the direction of the transient lateral Coriolis forces generated by the forward velocity of their reaches. With additional reaches, subjects soon reach in straighter paths and become more accurate at landing on target even in the absence of visual feedback about their movements. Two factors contribute to this adaptation: first, muscle spindle and golgi tendon organ feedback interpreted in relation to efferent commands provide information about movement trajectory, and second, somatosensory stimulation of the fingertip at the completion of a reach provides information about the location of the fingertip relative to the torso.

Acceleration↗

Proprioceptive feedback in locust kicking and jumping during maturation.

Campaniform sensilla monitor the forces generated by the leg muscles during the co-contraction phase of locust (Schistocerca gregaria) kicking and jumping and re-excite the fast extensor (FETi) and flexor tibiae motor neurones, which innervate the leg muscles. Sensory signals from a campaniform sensillum on the proximal tibia were compared in newly moulted locusts, which do not kick and jump, and mature locusts which readily kick and jump. The activity pattern of FETi during co-contraction was mimicked by stimulating the extensor tibiae muscle. Less force was generated and the spike frequency of the sensory neurone from the sensillum was significantly lower in newly moulted compared to mature locusts. Depolarisation of both FETi and flexor motor neurones as a result of sensory feedback was consequently less in newly moulted than in mature locusts. The difference in the depolarisation was greater than the decrease in the afferent spike frequency suggesting that the central connections of the afferents are modulated. The depolarisation could generate spikes in FETi and maintain flexor spikes in mature but not in newly moulted locusts. This indicates that feedback from the anterior campaniform sensillum comprises a significant component of the drive to both FETi and flexor activity during co-contraction in mature animals and that the changes in this feedback contribute to the developmental change in behaviour.

Aging↗

Proprioceptive input resets central locomotor rhythm in the spinal cat.

The reflex regulation of stepping is an important factor in adapting the step cycle to changes in the environment. The present experiments have examined the influence of muscle proprioceptors on centrally generated rhythmic locomotor activity in decerebrate unanesthetized cats with a spinal transection at Th12. Fictive locomotion, recorded as alternating activity in hindlimb flexor and extensor nerves, was induced by administration of nialamide (a monoamine oxidase inhibitor) and L-DOPA. Brief electrical stimulation of group I afferents from knee and ankle extensors were effective in resetting fictive locomotion in a coordinated fashion. An extensor group I volley delivered during a flexor burst would abruptly terminate the flexor activity and initiate an extensor burst. The same stimulus given during an extensor burst prolonged the extensor activity while delaying the appearance of the following flexor burst. Intracellular recordings from motoneurones revealed that these actions were mediated at premotoneuronal levels resulting from a distribution of inhibition to centres generating flexor bursts and excitation of centres generating extensor bursts. These results indicate that extensor group I afferents have access to central rhythm generators and suggest that this may be of importance in the reflex regulation of stepping. Experiments utilizing natural stimulation of muscle receptors demonstrate that the group I input to the rhythm generators arises mainly from Golgi tendon organ Ib afferents. Thus an increased load of limb extensors during the stance phase would enhance and prolong extensor activity while simultaneously delaying the transition to the swing phase of the step cycle.

Afferent Pathways↗

Multichannel transmission of proprioceptive input to motoneurons.

A model has been developed to simulate the parallel channels of muscle spindles and their monosynaptic connections to a homonymous motoneuron in the turtle. Input to the model is muscle length and beta stimulation, output is motoneuronal membrane potential. Quality of transmission is greatly dependent upon dispersive properties of the system. The contributions of different dispersive features are compared and also cumulative effects are considered. Reference is made to conditions which are found in actual movements.

Action Potentials↗

Extraocular proprioceptive signals affect ocular motor activity neither directly nor parametrically in the presence of optokinetic or vestibular stimulation in the frog.

Direct and parametric effects of stretch receptors in the extraocular muscles on abducens nerve activity were investigated in the unanesthetized immobilized frog. Horizontal passive rotations of one eye in the physiological range (+/- 5 degrees) did not elicit responses in the activity of abducens nerve on either side; however, larger rotations or pull of one eye evoked long latency direction-unspecific responses simultaneously in both nerves. When the animal was stimulated vestibulary in the horizontal plane with sinusoidal or constant acceleration, abducens activity was not altered in correlation to passive eye movements in the physiological range. Similarly, the activity of either nerve evoked by simultaneous or preceding optokinetic stimulation of one eye with constant pattern velocity was not modified by passive rotation of the contralateral eye.

Abducens Nerve↗

Responses of spiking local interneurones in the locust to proprioceptive signals from the femoral chordotonal organ.

The responses of spiking local interneurones of a ventral midline population in the metathoracic ganglion of the locust, Schistocerca gregaria, to controlled movements of a proprioceptor, the femoral chordotonal organ (FCO) in a hindleg, were revealed by intracellular recording. Afferents from the FCO which signal specific features of the movement or angle of the femoro-tibial joint, can make direct excitatory synapses with particular interneurones in this population (Burrows 1987a). Some interneurones in this population are excited only by flexion, some only by extension, but others by both flexion and extension movements of the femoro-tibial joint. Interneurones excited by one direction of movement may be either unaffected, or inhibited by the opposite movement. The balance between excitation and inhibition is determined by the range over which the movement occurs, and can increase the accuracy of a representation of a movement. The response of some interneurones has tonic components, so that the angle of the joint over a certain range is represented in the frequency of their spikes. Different interneurones respond within different ranges of femoro-tibial angles so that information about the position of the joint is fractionated amongst several members of the population. These interneurones respond to repetitive movements, similar to those used by the locust during walking, with bursts of spikes whose number and frequency are determined by the repetition rate and amplitude of the movement. A brief movement of the FCO may induce effects which persist for many seconds and outlast the changed pattern of afferent spikes. The sign of such an effect depends upon the preceding history of stimulation. Other interneurones respond only to movement so that their response is more phasic. The velocities to which they respond fall within the range of those generated by twitches of the flexor and extensor tibiae muscles and the movements of the tibia during locomotion. Some interneurones respond only to a specific range of velocities because they are inhibited by all other movements. Some interneurones respond to repetitive movements with reliable bursts of spikes, whilst in others the frequency of spikes may be raised but may contain no cyclical information.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials↗