Proprioceptors and the flight motor pattern

Locusts have a large array of sensors that report back to the central nervous system on the mechanical effects which the commands it issued slightly earlier caused. This is necessary because the effects of muscle contraction are not totally predictable. A flying locust might, for example, experience a gust of wind which causes its course to deviate. When it deviates, the wings on one side of the body might move up and down more than those on the other side for a few wing-beat cycles.

A large number of proprioceptors monitor movements of each wing and two types have been most intensively studied. The first consists of just one sensory receptor cell, called the wing hinge stretch receptor. Its cell body is embedded in an elastic strand which spans the joint of the wing with the side wall of the thorax. The large calibre of the axon of the stretch receptor has enabled experimenters to record from it, even during tethered flight. Wing elevation excites the stretch receptor and it fires a burst of spikes during each wing-beat cycle, with the number of spikes reporting the extent of elevation (Fig. 7.6a). The second sense organ is called the tegula, and this

Figure 7.6 Proprioceptors and locust flight. (a) Spikes in a forewing stretch receptor recorded simultaneously with up and down movement of the wing and an EMG from a hindwing depressor muscle. (b) Arrangement of an experiment in which a locust controls its angle of flight into the wind by varying the interval between spikes in two flight motor neurons, here one on the left and the other on the right. Wire electrodes record EMGs and, after amplification, the time difference between excitation of the two motor neurons is measured for each wing-beat cycle. The time difference is compared with a predetermined reference value and if the two are equal, flight course is unaltered. If there is a difference, the motor turns by a few degrees to alter the direction of flight relative to the wind. (c) Recordings from an experiment like that in (b), in which spikes from right and left motor neurons 129 were recorded. The reference value for the right-left delay switched every 25 s between 1 and 2 ms. Quite rapidly, the locust adjusted the delay between right and left spikes to follow the reference value and, after an initial swing, it maintained a flight direction more-or-less straight into the wind. (a from Mohl, 1985; b and c modified from Mohl, 1988; copyright © 1985, 1988, Springer-Verlag.)

contains a number of stout hairs borne on a cuticular pad beneath the base of the wing. Inside this pad is another proprioceptive sense organ called a chordotonal organ. The hairs of the tegula are brushed and excited by wing depression. The stretch receptor and the tegula, therefore, respectively monitor wing elevation and depression. Other aspects of wing movement are also monitored; even the tiny wing veins bear tension transducers on their surfaces.

Both the stretch receptor and sensory cells of the tegula make direct, monosynaptic connections onto flight motor neurons and interneurons (Burrows, 1975; Pearson & Wolf, 1988). The stretch receptor excites almost all of the depressor motor neurons on the same side of the body as its wing. This means that when the wing is elevated, excitation of the stretch receptor will enhance excitation of the depressor motor neurons whose action opposes the elevation. If the wing is elevated more strongly than usual, the action of this proprioceptive reflex is to ensure that the depressors are excited more quickly than usual. The effect is to restore wing movement to the usual or preferred pattern. Similarly, the tegula excites wing elevator motor neurons when the wing is depressed.

In early experiments, attention was focused on the effects that stretch receptors have on the flight rhythm. When stretch receptors were removed, the flight rhythm dropped, and could be accelerated again by stimulating the axon of a stretch receptor. Recent experiments have shown that these, and other proprioceptors, play a vital role in ensuring that the flight motor output is appropriate for achieving stable locomotion. Intracellular recordings from flight motor neurons show characteristic features that are due to input from particular proprioceptors (Pearson & Wolf, 1988; Pearson & Ramirez, 1990). Elevator motor neurons, for example, show two phases of excitation during a wing beat, with synaptic inputs from the tegula sensory neurons preceding excitatory input from interneurons. The wing proprio-ceptors are, therefore, deeply embedded into the circuitry that generates the flight pattern.

The central pattern generator and proprioceptive feedback loops work together subtly to ensure that the animal's motor output is continually adjusted to maintain its desired course. This can be illustrated by some experiments conducted by Bernhard Mohl (1993). If a locust is tethered to a holder which allows it to swivel to the left or right, the locust will continually adjust its angle of yaw so that it flies straight into an air stream. In his experiments, Mohl did not allow the locust to provide its own power for changing its angle of yaw but used a small motor attached to the holder to twist it (Fig. 7.6b). Rotation of the motor was controlled by a computer, which measured the time interval between spikes in the EMGs recorded from two different flight muscles and compared this with a reference value selected by the experimenter. The locust, therefore, could control its own yaw angle by slight variations in the interval between spikes in the two motor neurons, which were often the left and right hindwing muscles 129. In the experiment shown in Fig. 7.6c, the first reference value chosen was a time difference of 2 ms between spikes in the left and right 129 motor neurons, so that the locust remained on a flight course straight into the wind when it maintained this interval. The reference value was then switched to 1 ms, and the locust quite rapidly reset the interval between spikes in the left and right motor neurons. Whenever the reference value was altered, the locust reset the interval between spikes in the two selected motor neurons. Different pairs of muscles were selected in a series of experiments.

These experiments have revealed a degree of plasticity in the locust nervous system which was unexpected. The locust cannot know which pair of motor neurons the experimenter has selected for a particular experiment. This means that the locust must be able to compare the results of varying the timing among different pairs of motor neurons before discovering which ones are effective in maintaining course. Cutting the pair of muscles selected destroys the ability of the locust to maintain course in this way, which shows that proprioceptive feedback about the mechanical effects of muscle contraction is required. We do not yet know which proprioceptors are involved: the stretch receptor and tegula hairs both report movements of skeletal elements rather than individual muscle contractions;and flight muscles are not known to have sense organs similar to the muscle spindles of humans embedded in them. Mohl's experiments show that small, continual variations in the motor pattern are important because they allow flexibility in the most effective pattern at maintaining course. The central nervous system does not generate an unchanging, 'perfect' motor pattern; the pattern is tuned through the action of proprioceptors. Instead, we can view one important role for proprioceptors as participating in selecting the most effective program for maintaining a desired course. The ability to make continued, small adjustments to the motor output means that the pattern can be continually updated, and rapidly adjusted to particular conditions. For a locust, these conditions would include wind direction, and turbulence caused both by the wind and neighbouring locusts in a swarm. A similar strategy is becoming adopted by engineers in designing control systems for robots, because it provides a way to compensate for inevitable inaccuracies in manufacturing. It is difficult, for example, to ensure that the friction in wheel axles on the left and right sides is exactly balanced.

Essentials of Human Physiology

Essentials of Human Physiology

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