I. INTRODUCTION

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Control of posture and locomotion is closely linked to control of gravitational load. All animals, which have to deal with this problem, rely on a variety of more or less specialized receptors. Activation of these receptors is essential for some human postural reactions (162, 163) and for the control of the intensity and duration of extensor activity bursts (stance phase) during walking in different groups of animals (97, 260, 471). This is possible because during movement the input from load receptors interacts with command signals and rhythm-generating circuitry. In fact, activation of these receptors can even determine the choice of the appropriate coordinated pattern.

One spectacular example of the effect of frictional load has been given by Wendler et al. (530) when studying the hemipterus Nepa rubra. This insect walks in a classical alternating tripod coordination (at least 3 legs on the ground at any time), with alternation of the legs of the same segment. In this case, the stance phase is normally longer than the swing phase. When swimming, all legs are in phase and the swing phase is significantly longer than the stance phase. It has been possible to design experimental situations in which the frictional load is intermediate between the ground and the water condition (walking on mercury or on a slippery surface). In this latter case, swing and stance are equal in duration, and both in-phase and out-of-phase locomotor patterns were used in alternation. This demonstrates that load, which is important during stance, is crucial in controlling the interleg pattern. Similar load-dependent switches in interlimb coordination have been described in the fishing spider Dolomedes, which rows on the water surface and walks on land (19).

There are several reasons why this review is needed. First, the definition of load receptors should be reevaluated. In mammalian physiology, the question of load receptors is often reduced to a discussion of a single type of receptor, namely, the Golgi tendon organ (GTO) of extensors. However, when a limb is loaded during stance, a wide variety of receptors are activated, including cutaneous receptors of the foot, higher threshold force receptors, and spindles from stretched muscles (105, 106, 460). To what extent, and by what means, are these diverse sensory inputs combined at the spinal cord level to inform the animal about load? Should one make a distinction between receptors involved in the detection of gravitational versus inertial versus frictional load? In arthropod physiology, a large amount of data are now available on load receptors and load-compensating reflexes. Previously most attention has been given to position and movement detectors [such as the hairplates, the muscle receptor organ (MRO), or the chordotonal organs (CO)], but more recently, there has been an increasing interest in the cuticular receptors, such as the campaniform sensilla, which may act as typical load receptors. Moreover, the role of passive load-compensating mechanisms should be considered.

Second, a review on the mechanisms of load regulation is timely. In the cat, the discussion of load compensation in leg muscles has long been dominated by the concept of autogenic inhibition (negative force feedback) from Ib afferents of GTO from leg extensors. However, the view on Ib feedback is rapidly changing because recent experiments have shown that this inhibition is very short-lasting; therefore, its functional importance is in doubt (343, 344). On the other hand, support is growing for alternative ideas based on experiments testing the function of load feedback under conditions related to locomotion (412, 416, 534). In particular, the proposal has been made that, under such conditions, the Ib input from extensors inhibits flexors and facilitates extensor activity in the cat (191). The evidence in favor of this proposal has rapidly accumulated over the last few years (111, 246, 415). Moreover, additional new data are presented to show that these flexor suppressive effects are due to Ib rather than Ia input from extensors. On the basis of these findings, it is concluded that activity from Ib afferents from extensors reinforces the ongoing extensor activity during the stance phase and can block the initiation of swing. Cutaneous afferents from the foot can have a similar effect. Hence, different types of load receptors can signal unloading, and this might be essential for the termination of stance. In addition, other afferent input (presumably primarily related to limb position) can facilitate the transition to swing (260). Recently, these findings have attracted the interest of researchers working with patients with spinal cord injury, because it has become possible through intense training to regain some locomotor activity in these patients, and this rhythmic efferent output can effectively be manipulated by changing the load level (168, 277, 388). These new training schemes are based on the knowledge that the above-described load-compensating reflexes to extensor muscles (111, 191, 246, 415) can be effective not only in spinal cat (274, 277, 364) but also in spinal human.

As in the cat, it has been found that afferent activity from load receptors in arthropods feeds into pathways that were described as substrates for negative and positive force feedback. These feedback mechanisms play a crucial role in phase-switching during locomotion. Moreover, both in arthropods and in cats, the direct influence of this input on the central sites involved in the generation of locomotor output has been demonstrated by experiments involving rhythm entrainment or resetting (20, 412). The crucial question is how the activity in these different load feedback pathways is regulated. Does it depend on the task (locomotion)? During such a task, is the modulation of activity a function of the phase of the movement? To what extent is positive force feedback a sensible interpretation?

Although some reviews are available that describe specific load receptors and their reflexes (e.g., Refs. 20, 314, 442, 513), there have been few attempts to incorporate this knowledge with respect to behavior (283, 436, 457, 534). Moreover, a thorough comparison with human neurophysiological data is seldom made. In comparison with other species, bipeds such as humans face the problem of a reduction in the number of supporting limbs. For our review, we have considered three animal groups where load is a crucial control parameter: the arthropods, which include hexapods, octopods, and even multipods; the mammalian quadrupeds like the cat or the rat; and the bipedal human. In the past, the application of a similar comparative approach has proven to be fruitful in detecting some striking similarities in basic principles used to handle gravitational load during walking (93, 128, 412, 416, 556). The different load-compensating mechanisms are then discussed, along with their role in postural reactions and in regulating the phases in walking. The data are considered within a theoretical framework of feedback regulation of position, force, and stiffness.

Another point that sometimes leads to misunderstanding is the definition of positive and negative feedback. For example, a classical closed-loop controller works with negative feedback, i.e., the actual value x_act to be controlled is measured by sensory systems, and this value is then compared with the desired value to determine the error signal (Fig. 1A).

View larger version (17K): [in this window] [in a new window]   Fig. 1. A: scheme showing a negative-feedback controller. Xref, reference input, desired value; Xerr, error signal; Xsens, actual value as measured by sense organ. B: 2-joint arm tip of which should be moved along x-axis on horizontal surface. C: 2 negative-feedback systems controlling position (pos; I) or force (f; II). For explanations, see text.

This comparison is done by subtracting the actual sensed value x_sens from the desired value x_ref. For this subtraction, the sign of the sensed value has to be inverted, giving rise to a description in terms of negative feedback. Depending on the sign of the deviation, such a feedback control system can, however, provide actions with different, i.e., positive or negative sign, depending on the sign of the error signal x_err. The overall gain G of the feedback system is C/(1  C × S), where C is the gain of the forward part of the loop (controller plus actuator, Fig. 1A) and S is the gain of the recurrent part (sensor, feedback transducer). As long as the disturbance is zero, the reference value determines the actual value according to x_act = G × x_ref. If the desired value of such a closed-loop controller is fixed, this system provides the basis for the so-called resisting reflexes. As an example, take a simple joint moved by two antagonistic muscles, a levator and a depressor muscle. Assume that the joint is in a resting position such that both muscle forces (plus gravity) balance each other. If by an external disturbance the limb is lifted, for example, the depressor muscle will be activated to resist this disturbance. Such a system could also be used as a servocontroller, i.e., a feedback controller, the set point (reference input, desired value) of which is not fixed but can be changed by higher centers. The servocontroller might, for example, be used to activate the depressor to move the limb downward. If the limb is loaded such that it does move only slowly or not at all, the error signal increases as the set point is moved to values corresponding to more lower positions. This increases the strength of the motor output, and therefore, the load of the leg is further increased. This observation might lead to the interpretation of an "assisting" reflex or positive feedback, because increase of load leads to higher muscle activation that further increases the load. However, this assisting effect is based on a system with negative feedback.

In addition to position, or its higher derivatives velocity or acceleration, the controlled variable might, for example, be force. To simplify the discussion, the nature of force versus position control requires consideration. When a leg or an arm has to be moved through free space, the movement of the hand or the leg tip need not necessarily be specified in fine detail. Therefore, different control principles like velocity control, or soft or rigid position control, are applicable. The situation is different when the arm or the leg has to be moved under some mechanical constraints. Assume, as an example, that the tip of a two-joint arm should be moved along a horizontal line while gliding on a horizontal surface (Fig. 1B). Assume that the tip of the arm is controlled by means of a rigid position controller, for example, an "integral" controller (i.e., controller C in Fig. 1A, having the property of an integrator; see also Ref. 130). Then a small deviation of the horizontal line, be this caused by an uneven surface or only by inexact sensor data, would cause the tip to either lose contact with the surface or the controller would produce maximum force to push the tip hard against the surface to reach the ideal horizontal line (assuming the above-mentioned I-controller or a position P-controller of high gain). To avoid these problems, a control system permitting compliant motion is required. Compliant motion means that the movement trajectory is modified by contact forces or tactile stimuli occurring during the motion.

Compliant motion can be obtained in two ways that are called passive and active compliance. For passive compliance, elastic elements are used which in biological systems are in the form of elastic muscles. Tendons and skeletal structures may also contribute to passive elasticity of the limb. Using an elastic element, the problems mentioned above could be solved. However, the force cannot be controlled properly. It rather depends on the size of the disturbance. In active compliant systems, the degree of compliance can be adjusted according to variable requirements. Two different principles will be discussed, namely, "soft" position control (using a proportional controller) and force control. Both will be explained using a single joint system. Figure 1C shows a limb that can be moved by two muscles, here symbolized by two springs (with adjustable stiffnesses). A position measuring sense organ (I) is attached to the joint to measure the actual position of the limb. This value is compared with a reference value, the desired position pos_ref, by means of a subtraction (negative feedback). The resulting error signal pos_err is given to the controller, which in this case represents a proportional element (P controller). The output of this controller determines the activation of the two muscles. A disturbance, for example, an external weight attached to the limb, moves the limb downward, thereby increasing the error signal. This in turn increases the activation of the muscles, in this case the upper "levator" muscle to compensate for this disturbance effect. Because the controller is a proportional element, the compensation is not complete, but proportional to the size of the disturbance. Therefore, the whole feedback system acts like an elastic element, whose stiffness can, however, be adjusted by changing the gain of the feedback loop (this form of active compliance is sometimes called impedance control, Ref. 47). This system represents a negative-feedback system controller for the position of the joint. In arthropods, joint position may be measured by hair plates or chordotonal organs, for example. Correspondingly, muscle spindles or joint receptors could alternatively be used to measure joint position in vertebrates.

Figure 1C, top, shows another control system, namely, a force feedback controller. A small elastic element (II) is attached to the end of the arm. This is bent when the limb is loaded by, for example, a weight as symbolized by the arrow "dis" in Figure 1C. This element can be interpreted as a sensor of the force or the load. In arthropods this could be realized by campaniform sensillae, cuticular stress detectors, or other organs. In vertebrates, Golgi organs are the main sensors. This sensor signal can be compared with a value representing the desired force f_ref to determine the error signal f_err. Via a controller, this signal influences the muscles. When in this case the same disturbance force (limb pushed downward; see arrow "dis") is provided as has been considered in the case of the position controller, the levator muscle activation now decreases to move the limb downward, i.e., away from the disturbance input, because this controller tries to maintain a constant force value as measured by the sensor. Therefore, although we again have a negative-feedback system, in this case of force feedback, the reaction to the same disturbance input has a different sign.

Therefore, if one is not aware of the modality of the relevant sense organs, one may interpret this effect as to result from a positive position feedback. An ideal position sensor is compliant (Fig. 1C, I), whereas an ideal force sensor is stiff (Fig. 1C, II). Correspondingly, an ideal position tranducer is in series, an ideal force transducer in parallel with the moving element. However, there are also somewhat compliant systems like impedance-controlled muscles, whose muscle spindles could be used to transmit information about force. Therefore, the distinction is not always immediately clear.

At first sight, one might assume that a given joint could not at the same time be under force and position control because, as in the example explained here, both controllers act in opposite directions. However, both controllers may cooperate sensibly. When, for example, the force controller of the levator-depressor system shown in Fig. 1C is used to carry a given weight (represented by the arrow "dis" in Fig. 1C) against gravity and therefore develops an upward directed (levator) force, and, at the same time, the position controller is used to lift the limb upward, then both controllers cooperate to excite the levator muscle.

There are of course also true positive-feedback systems, but these can show different behavior. Let us consider a position controller. In the case of negative feedback, the movement stops when the desired value, or set point, is reached. In the case of positive feedback, the overall gain is C/(1  C × S). For C × S < 1, the system behaves in principle like a negative-feedback system but has a higher overall gain for given values of C and S. For C × S 1, the system is instable, i.e., the movement continues infinitely and possibly with increasing velocity and stops only if an external reason is provided or a saturation level is reached. (Correspondingly, in the case of positive force feedback, the force should continuously increase.) A critical test for positive feedback is to experimentally change the direction of the movement of the actuator output by application of a disturbance, in our example by moving the leg. For positive displacement feedback, the actuator should now augment this new movement, whereas for negative feedback it should continue to follow the old direction (e.g., Ref. 467).

The theoretical basis of positive feedback has not been studied in great detail because positive-feedback systems are generally considered to show problems concerning stability. However, very recently it was shown that proportional systems with positive feedback cannot only be stable but can show interesting properties (for positive force feedback, see Refs. 437, 438; for positive displacement feedback, see Refs. 133, 467). Particularly elegant solutions that can explain puzzling experimental results are provided by concomitant positive force feedback and negative displacement feedback (Refs. 437, 438; see sect. VII). Application of a positive displacement feedback with a loop gain of ~1 (C × S 1) can be used to solve several problems occurring when mechanically coupled joints have to be coordinated. This is possible when the instability is "tamed" by the introduction of a high-pass filter into the loop (133, 467).

The importance of this point on terminology can be judged by inspection of the current literature on Ia and Ib effects in the mammalian system. As will be described further in section VIB, it is often argued that Ia afferents cause reflex effects consistent with negative feedback and Ib afferents provide effects in line with positive feedback, at least during the stance phase of gait. It is important to realize that in fact, both types of feedback can assist each other during the stance phase, since they both only provide basically for facilitation of extensor activity assuming the extensors actively lengthen. Hence, they both can be seen as assisting reflexes from the point of view of extensor contractions and load compensation, because the sign of the action depends on the sign of the error signal. In this way, particularly elegant solutions that can explain puzzling experimental results are provided by concomitant positive force feedback and negative displacement feedback (437, 438; see sect. VII).

Another possible misunderstanding refers to the term open-loop control. This is meant to describe a system that does not rely on feedback signals, for example, a targeting movement with dorsal roots cut, and is sometimes also called feed-forward control. In reality, however, this control signal is usually influenced by sensory signals, for example, visual input, which provides feedback of target position. Therefore, a so-called feed-forward control might, on a higher level and maybe on a different time scale, also correspond to a feedback controller (136).

The above-mentioned problem of control of compliant motion could be solved by a force controller or by a soft position controller, or in some cases as mentioned, by a combination of both. A problem not addressed up to now is that, in a realistic situation, the movements of several joints have to be controlled. Thus the system has several degrees of freedom. The control task might then be complicated in such a way that the task differs for the different degrees of freedom. For example, the task described in Figure 1B has two degrees of freedom: one along the y-axis and the other along the x-axis. This task requires a compliant control in the direction of the vertical (y) axis as mentioned above. However, along the horizontal axis, a rigid position control might be advantageous because a rigid position control helps to minimize errors. How can both goals be achieved? The classical engineer's solution to this problem is the so-called hybrid control; movement in the horizontal direction is under position control, whereas movement in the vertical direction is under force control. In the case of a leg in stance, we have just the opposite situation. Movement in the vertical direction (control of body height) is under position control, but for movement along a horizontal axis, the leg might be under force control (133). It is, however, not always possible to attribute these two tasks to separate joints. Usually all joints can contribute to both tasks making a hybrid controller a possible, but complicated system (47).

	II. LOCOMOTOR BEHAVIOR AND LOAD

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Walking is a repetition of successive steps. Each step is composed of two phases. In forward walking during the swing phase, the leg is lifted from the ground and is moved by its muscles against its inertial load. At the end of this phase, the leg reaches an anterior extreme position (AEP). During the stance phase, the leg is on the ground supporting the gravitational load of the body and propelling the animal, i.e., acting against inertial and frictional load. At the end of this phase, the leg reaches the posterior extreme position (PEP). In invertebrates, but also in vertebrates which use other modes of locomotion with a specific locomotor apparatus (like a paddle for swimming or a wing for flight), the two phases are also present and often named power stroke for the corresponding stance phase and return stroke for the corresponding swing phase. The movement during the stance phase has often been compared with a slow ramp, whereas the movement during the swing phase to a ballistic action (152). Because body weight depends on the surrounding medium, the importance of load is very different in these various motor activities. Gravitational load is especially crucial in terrestrial walking, whereas it is relatively less important during locomotion under water, where frictional load is an important element.

The role of load is particularly well illustrated in animals that locomote in various media. For example, amphibious animals can move equally well in and out of water. The crab, Carcinus maenas, walks laterally most of the time with four pairs of legs. The legs in the direction of walking are the leading legs; those pushing the body behind the cephalothorax are considered trailing legs. In seawater, the crab's weight is about seven times less than on land. In general, the cadence under water is faster than on land. The basic motor pattern, however, is somewhat similar in both cases with respect to muscular synchronization and opposition. A careful study of motoneuronal discharge demonstrates significant differences in the two media (101). On land, power stroke muscle discharges lasted longer and involved the activation of additional motor neurons in muscles that are innervated by several motor neurons. Under these conditions, maximal discharges occurred at the beginning of the burst and reached frequencies as high as 200-350 Hz. Such discharge rates are sufficient to increase significantly the muscle contractions needed to support the animal on the ground.

In walking stick insects, load influences were produced experimentally in various ways. The direction of gravity changed by letting the animals locomote under different conditions (e.g., walking on a horizontal plane or on a vertical plane and hanging upside down from a horizontal beam, Ref. 120). The latter situation was recently also studied with cockroaches and the locust (183, 346). The frictional force was changed by letting the animal walk on mercury (255) or on a slippery oil plate (138, 213), or applying friction to the treadwheels (227). Furthermore, the inertia of the wheel was changed (252), or different external torques were applied to the wheel (153, 227, 228). Because the mass of the body has to be carried during stance, load influences are to be expected to affect leg movement during stance, but tests with loads applied specifically during the swing show that it, too, compensates well for experimental changes. Generally, these load influences affect the position of the AEP and the PEP as well as the duration of the swing.

For example, in the rock lobster, the removal of load receptors by autotomy of the legs is assumed to cause the activity in the remaining stump to switch from an alternating pattern, such as seen during walking, to an activity profile in phase with the other legs, as is seen in a behavior in which load receptors are minimally activated, namely, during swimming. The direction of walking can also be determined by load. The grain weevil, Sitophilus granarius, which in complete darkness has a circling behavior on a horizontal surface, is able to go straight when the animal walks on inclined surface (529). In that case, it has a preferred direction (downward) due to the activation of the receptors of the leg which indirectly measure the direction of gravity. Another example of the effect of frictional load has already been given in section I, namely, the change in coordination of Nepa rubra legs from swimming to walking, dependent on frictional load (530).

Load afferent input can be decisive in triggering specific types of locomotor behavior. In the cockroach it has been demonstrated that there are some interneurons (IN) that can induce flight if load-related tarsus information is absent and walking if it is present (447). Similarly in the crab, the combined activity of four groups of equilibrium IN is necessary to ensure bilaterally organized movement, and the input to these IN determines the type of motor output. Fraser et al. (231) suggested that these IN can trigger both swimming and walking. The crab has some specific load receptors in the dactyl (distal part of the leg), the stimulation of which induces walking activity. In the absence of this sensory activity, swimming is the default motor output (41).

Comparing different motor behavior in the ontogenesis of birds, Bekoff (36) has shown that in patterns where forces are exerted, return stroke and power stroke durations in the step cycle are very different, while they differ only slightly when the load is limited.

In mammals, comparable differences can be found between walking and swimming. Both types of locomotion use similar motor programs, but the relative timing of the main phases depends on the load. In rat, for example, the flexion phase of swimming and walking has many elements in common, including similar electromyogram (EMG) activation patterns. In contrast, the extension phase is extremely short in swimming as compared with walking and followed by an intermediate period of knee flexion and selective activation of semitendinosus muscle activity (401). If one assumes that the muscles are driven to their maximum contraction rate, swing bursts have similar durations and timing in walking and swimming, whereas the extensor bursts are totally different (269) because of the presence or absence of ground reaction forces.

Iles and Coles (311) have extended these experiments, studying decerebrate rats. Locomotion was induced at controlled step rates by electrical stimulation of the mesencephalic locomotor region. Animals were running on a freely moving wheel to which frictional loads could be added, which caused an increase in the extensor burst duration. This increase was 10% for semimembranosus and vastus lateralis and 40% for the other extensors. For muscles with double bursts, such as the semitendinosus, the extensor phase activity is prolonged. In contrast, when gravitational load was reduced by performing similar experiments in a tank of water, the duration of the extensor bursts was reduced by 35% while flexor bursts increased by 60%.

Hence, various muscles can react very differently to loading. Probably the best studied example is the difference between various muscles belonging to triceps surae. In the guinea pig, Gardiner et al. (237) found that loading the animal (through a halter-pulley apparatus) led to a much more dramatic increase in the EMG activity of lateral gastrocnemius (LG) than of soleus. Varying speeds give the same type of results in cats (426), with a higher contribution of gastrocnemius than soleus under conditions where more force is required. In humans, the same basic difference between LG and soleus is seen with changes in speed (199).

In cats, the role of gravity on walking has been studied extensively using locomotion on inclined surfaces (292, 426, 503). As expected, the activity in extensor muscles greatly increases during uphill walking. Interestingly, however, during downhill walking, Smith and Carlson-Kuhta (503) found that it was the flexors and not the extensors that dominated the stance phase. In this respect, it is worthwhile mentioning that some animals use flexors as antigravity muscles. The slow loris is a primate that uses arboreal locomotion. It climbs in trees and can progress along the branches either in an upright or in an inverted position. A combined kinematic and EMG study (183, 326) demonstrated that the upside down sagittal pattern is a mirror image of a pronograde upright pattern. The flexors acted as antigravity muscles when the animal was in an inverted position. Propulsion was still achieved through activity in extensor muscles. This is a necessary consequence of the physical situation and is therefore more or less also found in climbing insects (120, 183).

Humans can commonly bear loads of up to 70% of their body mass during walking (297, 369). In the case of African women of some tribes, the task of load-bearing on the head has resulted in some remarkable adjustments (369). These women can carry loads of up to 20% of their body weight without increasing their rate of energy consumption. For other humans, as well as for horses, dogs, or rats, a similar increase in load results in an increase of ~20% in rate of energy consumption. When humans bear loads or walk uphill there is an increase in activation of extensor muscles (410). Inversely, when weight is reduced by body immersion, the EMG and postural reflex responses are reduced in ankle extensors (166). Similar gravity dependence is absent for ankle flexors, implying that proprioceptive input has a more dominant role in extensors than in flexors. The same conclusion was reached following a study on split belt gait, in which it was shown that the amplitude of the ankle extensor activity increased with speed despite constancy of step cycle duration, whereas this was less so for the ankle dorsiflexors (175). A similar asymmetry is apparent in an extreme form in the masticatory system, where stretch reflexes are present in the antigravity closers but not in openers.

In conclusion, load information is important in regulating different types of motor behavior. To understand this regulation, it is necessary to consider first how load is sensed in animals and humans and how this information is used to control the behavior. However, effects of load are not only counteracted by sensorineuronal mechanisms that use skeleton and muscles as mere executing organs. The physical properties of skeleton, tendons, and muscles by themselves already play an important role.

	III. PASSIVE LOAD COMPENSATION: BIOMECHANICAL FACTORS NOT RELATED TO LOAD FEEDBACK

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Even in the absence of reflexes, it is possible to resist changes in load. The stiffness of muscles is partly due to passive viscoelastic properties and partly to active contractions. Movement against a load (or "constraint") can follow either of two strategies. In the feedback strategy, information about load is used in real time to adapt the motor command. In the feed-forward strategy, an internal model of the constraint is used to adjust the compliance of the limb in anticipation of the contact force. The latter type of feed-forward control is undoubtedly very important, especially for fast movements [see, e.g., control of movements both of arms (378) and legs (504)], but this is not the main topic of the present review. In this section we limit ourselves to the discussion of some biomechanical elements that are important in load compensation in the absence of load feedback.

Some arthropods can maintain postural positions in the absence of muscle electrical activity (EMG) (548). This is due to the combination of passive elastic muscle tension and of particular biomechanical arrangements of the fibers. When measuring the length tension characteristics of muscles in various insects and crustaceans, Wilson and Larimer (538), Burns and Usherwood (64), and Hawkins and Bruner (284) demonstrated that there is a residual tension when the joints are at their extreme positions so that muscle develops force without energy consumption. It has been suggested that this resting tension could be sufficient to support the weight of the animals (548).

Another important feature for tonic postural activity is the catch property, as described by Wilson and Larimer (538) in the locust (Schistocerca gregaria). The extensor tibiae muscle is innervated by two excitatory motoneurons (MN), a slow (SETI) and a fast (FETI) extensor tibiae, respectively. The catch effect can occur when a high-frequency activation of the SETI axon is superimposed on a continuous low-frequency train. The response, which is only present in some of the fibers, takes the form of a tension plateau following the burst. This additional tension is maintained as long as the low-frequency activation is present. This is thought to be especially useful for the maintenance of posture and when the animal is climbing, in which case the SETI is continuously active at high frequency (64). During fast movements, the FETI MN are activated along with inhibitory MN that selectively speed up the relaxation after a contraction of the slow muscles. This is an elegant method of avoiding the slowing of the fast movement due to the long time constant of the slow fibers (see also Ref. 539).

Similarly, during crab walking, Ballantyne and Rathmayer (16) have shown that the tonic discharge of such an inhibitory MN (the common inhibitor, CI) plays a role in reducing the interburst tension of the rhythmically activated fibers. Bevengut and Clarac (40) confirmed this result in crab swimming. The frequency of such CI can increase with increasing activity. This can be due to the increase in sensory inputs, which are monosynaptically connected to the CI (85). This adaptive mechanism ensures that any increment in burst intensity due to increased load is compensated for by an increase in the burst relaxation mechanism.

In addition, it has been found that certain neuromodulators could play a crucial role in augmenting the muscular tension. For example, in the abdomen of the crayfish, 5-hydroxytryptamine (5-HT) increases the tension of flexors while octopamine has the same effect on extensors. Both substances, 5-HT and octopamine, act at two levels. As hormonal substances, distributed in the hemolymph, they facilitate the muscular contraction, whereas within the CNS, specific 5-HT or octopaminergic neuromodulatory neurons are involved in the control of flexor or extensor motor commands, respectively (336).

By analogy with arthropods, humans and other mammals require relatively little muscular contraction to achieve weight bearing during standing because of biomechanical factors (arrangements of ligaments and bones, intrinsic muscle properties such as its force-length and force-velocity relationships, and intrinsically stabilizing mechanisms in the musculoskeletal architecture; see Ref. 547). Small postural disturbances do not always induce active corrective reactions. Instead, these perturbations are compensated through passive viscoelastic properties of muscles and joints. When muscles are actively contracting, their stiffness increases, and they are even better suited to resist load changes. In fact, it has been argued that, under these circumstances, the muscle properties are more important for load compensation than stretch reflexes (257). Furthermore, for humans it has been shown that muscles can store and release mechanical energy (10), and this property can account for the high efficiency of muscles during gait (87).

On the other hand, it is clear that there are limits to the potential for load compensation by muscle on its own. For example, Nichols and Houk (398) showed that the stretch reflex in the decerebrate cat is well-suited to compensate for nonlinear properties of muscles and can complement these properties for the regulation of muscle stiffness. Muscles differ in their ability to resist loads either phasically or tonically. For vertebrates, as for arthropods, there are specialized slow muscles and/or muscle fibers that are resistant to fatigue (61, 327). There is some evidence that the MN supplying slow muscles can be inhibited actively during fast movements, such as during paw shaking in the cat (502). During postural tasks these slow fibers are essential, since they are specialized for providing high short-range stiffness for immediate compensation for postural perturbations (in advance of the reflex stiffness; see Refs. 368, 398).

In the cat triceps surae, motor units of the slow type produce markedly more force when they are activated by patterned stimulation of high frequency. The presentation of only a single interval, which is much shorter than the others (doublets), is sufficient to elicit this "catch property" (61). During locomotion of intact cats, doublets were found to be quite rare in a variety of muscles (294), but it is possible that they are used selectively to activate only slow muscles.

As in invertebrates, a potentially even more important mechanism is provided by the voltage dependency of the synaptic activation of MN. In the cat, Brownstone et al. (54) have demonstrated a strong "boosting" of the synaptic excitation from locomotor drive networks as MN are nearing their firing threshold in immobilized spinal cats in which rhythmic locomotor neural activity was induced by injecting L-dopa. The motor output of the latter type of preparation is commonly referred to as "fictive locomotion" (267, 325, 422, 550). The Brownstone et al. (54) results may explain why MN are recruited directly to high efficient firing rates during real locomotion, although, under different conditions, they have the potential to fire at lower rates as well (54, 55, 294, 483, 549).

	IV. RECEPTORS INVOLVED IN RECORDING LOAD

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What are load detectors? Often the term is used specifically to indicate receptors that measure muscle force. However, this definition is too narrow. When a standing animal receives a sudden unexpected increase in gravitational load, this load is not only perceived by muscle receptors sensitive to muscle contractions. Cutaneous receptors of the sole of the foot will be activated as well, along with all receptors that can sense the reduction in the joint angle of knee, ankle, or hip resulting from the extra loading (162). This includes not only joint receptors but also skin receptors signaling skin stretch and muscle length receptors (spindle afferents from extensors in the mammalian system). Hence, it is misleading to focus only on one type of receptor when discussing load-compensating reflex pathways. In this review, a distinction is made between main receptors (true load receptors and body load receptors) and accessory receptors (neuromuscular and joint receptors).

As we will see, afferent input from several receptors that may play a role in the detection of loading of the limb converge onto common IN. This illustrates that, for the regulation of load compensatory reflexes, the nervous system is interested in the ensemble of the afferent input related to loading rather than in the separate "private lines." This does not exclude the possibility that such precise information could be sent separately to higher centers for further processing. Hence, the question is not whether a given sensor is a load receptor or a force, length, or position receptor, since the same sensor can serve several of these functions. Nevertheless, all of these receptors are not equally sensitive to load, and it thus still makes sense to describe some of these receptors as being primarily load receptors (true load receptors, Table 1).

One should keep in mind that even a strict force receptor always measures changes in position because force can only be detected by its effect on movable, usually elastic material. Thus the difference between position and force distorting receptors is a quantitative not qualitative one. If the compliance of the elastic part is high, and therefore the movement is small, it is considered a force sensor, and vice versa. Therefore, in principle, a position receptor could also carry information concerning force. This is even more the case for those "position" receptors that also monitor velocity and acceleration, as described for the femoral CO of the stick insect (296). However, information on load changes could also be obtained when a change in load is not accompanied by a change in position.

In many arthropod species, changes in motor output to walking leg muscles are found that are related to the gravitational load they encounter during stepping and to dragged weight that impedes forward walking (crayfish, Refs. 101, 268; cockroach, Ref. 411; stick insect, Refs. 27, 28). In arthropods, load can be monitored in terms of exoskeletal strain (23, 44). Sensory cells inserted in the cuticule are real biological strain gauges present in insects, arachnids, and crustaceans. Although they vary in their morphological details, their design and arrangement provides for deformation even by small forces (22, 23). Moreover, internal proprioceptors can also be stimulated by load.

The main receptors in insects are the campaniform sensilla (CS). They are usually disposed in groups close to a joint and are composed of a bipolar cell innervating a small hole within the cuticle with dendritic terminals terminating in a cap of the exoskeleton. In the cockroach, the tibial CS have been studied in great detail by Zill and Moran (552-554). They respond to strain in the cuticle, resulting from forces due to muscle contraction and loading of the leg by the animal's weight (434, 435). In the tibia, there are two groups with different orientations. The proximal group, oriented perpendicularly to the long axis of the leg, responds mainly to dorsal bending of the leg and also to isometric contraction of the tibial flexor. The distal group, where cap orientation is parallel to the tibial axis, is activated by ventral bending and cuticular strains produced by contraction of the extensor muscle. Recently, it could be shown that both groups respond to the rate of force (446). The proximal group, for example, fires not only when the tibia is bent dorsally, but also when a force bending the tibia ventrally is released.

Probably the most important CS are situated at the coxa and the trochanter. In general, there are five groups of CS arranged next to the coxa-trochanter joint (cockroach, Ref. 435; locust, Ref. 309; stick insect, Refs. 28, 466, 469). Delcomyn (158) and Hofmann and Bässler (295) found tonic and phasicotonic units, but no pure phasic units, when recording from the trochanteral CS.

In the crustacean decapod leg, at least two different structures are involved in recording load (true load receptors, Table 1). The proximal cuticular stress detectors (CSD) (103) are composed of two elements. The first is located anterior and dorsal (CSD1) and the second is ventral (CSD2). They correspond to a soft cuticular region, innervated internally by a group of bipolar cells in a structure comparable to a true chordotonal organ. Klärner and Barth (331) have explained that the CSD2 is sensitive to deformation of the compliant cuticle. It is an accurate load receptor when the leg presses against the ground during standing or during the stance phase of the step cycle. These sensory cells are sensitive to local pressure of the cuticular soft patch (with either "on" or "off" responses or both). Most of the afferents give phasicotonic on responses.

The activity of on units increases with force, whereas it decreases with rising forces for the off units. The on units are also sensitive to low-frequency vibration, with an optimum around 10-30 Hz (331). The CSD1 has been studied only recently (370). Some of these sensory units have similar responses to those of CSD2, with on and off responses to pressure on the external patch, and they respond preferentially during the stance phase in walking. Another group of CSD1 afferents is sensitive to high-threshold stimulation. They are not likely to be involved in the routine perception of load, but they may be important in inducing autotomy (the loss of the whole limb, see Ref. 370). There are two advantages for these load receptors in insects and crustaceans to be located proximally in the leg. One is that neuronal conduction time is shortened when the sensors are near the base of the leg. The second is that for mechanical reasons the surface strain of a cantilever is strongest near its base.

In the crab, there are some very sensitive load detectors situated in the dactyl, which is the most distal segment (body support receptors; Table 1). These are the funnel canal organs (FCO) analogous to insect CS (22).

Two types are present with different positions within the dactyl. The most proximal ones are innervated by two sensory cells, grouped in one canal. They respond in a phasicotonic way to imposed load and encode vibrations at low frequency. One sensory cell is activated by dorsal stimulation, and the other by ventral stimulation. Hence, these proximal dactyl FCO receptors are directionally sensitive. During walking, these two units discharge more or less simultaneously during the stance phase. Nevertheless, the unit sensitive to dorsal bending always has a significantly higher discharge at the onset of stance (353, 354). The sensitivity of these units in response to applied force follows a sigmoid curve with the greatest change in firing occurring in the range of 25-70 mN (equivalent to the force produced by a mass of 3 to 8 g). A crab that weighs 60 g in air weighs only 8 g in water. Because the animal load is supported by six to eight legs, each leg exerts on the ground a range of force from around 10 mN when it is in water to up to 100 mN when it is in air. The FCO response curve demonstrates that the sensory units respond over the whole of this range.

The most distal FCO receptors are located at the tip of the dactyl. They are innervated by only one cell, and they only respond phasically. They encode vibrations at much higher frequencies than the proximal receptors (354). This difference in sensitivity may be related to topographical differences in the structure of the exoskeleton. Distally, the tissue is more flexible than proximally (lower calcium concentration). During walking, the distal phasic units are mainly active at the onset of ground contact. It is worth mentioning that these receptors are not only sensitive to externally applied load. Both CSD and FCO respond well to contraction of their surrounding muscles (levator and depressor for CSD, and opener and closer muscles for FCO).

In the arachnids, receptors that are comparable to those mentioned above have been described. For example, the lyriform organs and the CS of spiders (484, 485,486) have been described as true load detectors (Table 1).

Some receptors in arthropods are primarily involved in the registration of position and movement. Under certain loading conditions these receptors are activated as well because of the related changes in joint angles (see Table 1, accessory receptors). For example, in crustaceans as in insects, chordotonal organs are present at most leg joints (24, 27, 28, 30, 49, 65, 78, 214). The afferents firing during stance can be implicated in load compensation, since their firing rate is a function of the joint changes, partly induced by gravitational forces.

In insects, leg joint angles are also measured by hairplates or hair rows, external sensory hairs which are bent by the soft joint membrane when the leg joint changes its position. Such hair plates can monitor the position of the head relative to the body, and as such, they can be exploited to provide information concerning the direction of gravity (e.g., honey bee, Ref. 355; dragon flies, Ref. 385). Sensory hairs cover the whole surface of the body and the legs. These can detect local contact and may also monitor acceleration which, for example, is provided by loading a leg at the end of the swing movement.

In the femurotibial joint of the insects, different types of sensory afferents have been characterized, and recently, Matheson and Field (373) have summarized the complexity of the innervation of that joint in the locust. The structures involved are the CO, CS, multipolar receptors (28, 109, 516), and muscle tension receptors (for the subcoxal joint, see Ref. 308). In the crustaceans, similar structures have been studied in great detail. In the abdomen of the crayfish, each segment possesses two pairs of muscle receptor organs (MRO), located on either side of the dorsal midline, one phasic and one tonic. The phasic MRO is associated with rapid movement, and the tonic MRO provides a reliable signal of either muscle length or tension. In the legs of crustaceans, other neuromuscular proprioceptors have been described [e.g., the thoracocoxal muscle receptor (TCMRO) (76) or the myochordotonal organ (MCO) (see Ref. 78)]. Similar sense organs have also been found in insects (50).

All these proprioceptors (MRO, TCMRO, MCO) are coupled in parallel to independent contractile elements. Both the proprioceptor and the parallel muscle fibers are controlled by the same MN. These receptors can serve as peripheral references for the determination of a stopping point or set position. When shortening of the muscular part of the MRO is driven simultaneously with contraction of a parallel working muscle, the sense organ is not activated unless a resistive load is encountered during a movement and stretching of the receptor occurs.

Perhaps the receptors that are the most likely candidates for being true load receptors are the tendon receptor organs (Table 1; true load detectors). They are present in a fairly large number of crustacean leg segments (78, 281). They are not very sensitive to passive stretch, but their location is such that increases in muscle tension transmitted via the apodeme (an invagination of the cuticule on which the muscle fibers are attached) bring about increases in sensory discharge. The sensory cells are bipolar and grouped in clusters along the apodeme. If we compare them with the vertebrates, they differ from the GTO of the mammals in that they are not intimately associated with the muscle fibers themselves. They resemble more the receptors of the lizard (442), which lie in the tendon at a distance from the muscle-tendon junction. In crustaceans, this means that the tendon receptor organ may be sensitive to whole muscle tension as well as to a localized tension produced by the contractions of individual muscle fibers. Sensory cells connected to the muscle tendons have also been described for insects (28, 373).

Large groups of afferents are thus able to record load, and we have tried to limit the description to some major types. We may add, however, that loading of the whole body can be detected by specialized statocyst organs or gravity receptors that correspond to the otolith component of the vertebrate nonacoustic labyrinth (42).

B.  Vertebrates

1.  Exteroceptors

In mammals, one can distinguish two main load receptor types, one of which consists of body support receptors (Table 1). Cutaneous receptors of the sole of the foot can sense the deformation of the foot and ankle due to loading. Just after footfall there is a sharp rise of activity in the nerve supplying the foot pads in intact cats (193). Recordings from single afferents during the stance phase in the cat have shown that activity is generated selectively during stance even from skin areas that are not directly in contact with the ground (360, 362). Presumably, this is due to skin stretch, which can activate low-threshold mechanoreceptors. Such stretch-sensitive skin receptors could thus have a proprioceptive function. This is not only true for the foot but also for other parts of the body. For example, in humans, Collins and Prochazka (110) reported movement illusions evoked by stretches of the skin of the dorsum of the hand. In the monkey, it was shown that tactile activity during arm movements, avoiding direct skin contact, reached the primary somatosensory cortex (108).

In humans, the activity from cutaneous afferents during movement has been recorded through microneurography (59, 206, 305, 332, 366). These studies have confirmed that activity from mechanoreceptors can signal changes in joint angles and thus indirectly also loading. However, in general, this technique can only be used for small movements. For walking, a different technique is needed. To record the afferent activity from the foot during human walking, an implanted cuff electrode has been used (498). Activity in the sural nerve, which innervates the lateral side of the ankle and foot, was largest just after the foot hit the floor, although the innervation area of the nerve did not touch the ground. Moreover, a series of small bursts was seen throughout stance, coinciding with fluctuations in heel contact, as measured by separate sensors.

The role of the skin in load-compensating mechanisms has been most extensively studied in some forms of fine motor control. For example, due to the elegant work of Johansson and Westling (321, 322), we now know a great deal about the role of mechanoreceptors in the finger tips for precision grip and load detection. During precision grip, one produces forces that are slightly larger than the minimum required to hold an object (322). Insufficient force leads to slip, which is very effectively detected by skin mechanoreceptors. Compensatory reactions to sudden, unpredicted increases in load force occur with a latency of 40-50 ms in adults and 20 ms in young children (207), and it is thought that mechanoreceptors on the fingers are important for such reflexes. In general, grasp reflexes in infants show all the characteristics of a force "positive-feedback" system (see also Ref. 438 for review).

In mammalian muscles, the main receptors are spindles and GTO. Both are abundant in muscles that compensate for load during gait, and the number of both tends to covary in a given muscle (236, cited in Ref. 481). These proprioceptors have been mostly studied with respect to the reflex actions in the parent muscles, but there are good indications that this homonymous control is not the most important function. Scott and Loeb (481), for example, have argued that the distribution of spindles among human muscles seems better related to the need for information about the position of joints spanned by those muscles than to the control of the muscles themselves. Overall, the distribution shows a proximodistal gradient that is consistent with the observation that humans are better in judging positions of proximal than of distal joints (104, 276). For cats, some detailed measurements of the distribution of spindles have been made for some muscles (see, e.g., Ref. 444), but unfortunately there is no systematic survey available yet. On the other hand, the cat has been very thoroughly studied with respect to reflex connections (for a recent review, see Ref. 397).

Ever since Sherrington's work on cats, extensors have been equated with antigravity muscles in quadrupeds. Consequently, the Ib afferents from extensors are usually considered as the most important gravitational load receptors (Table 1; true load receptors). Golgi tendon organs are force-sensitive receptors that respond to muscle contraction and that have been studied most extensively as potential detectors of load (for review, see Ref. 314). They consist of capsules containing collagenous fascicles and intertwined sensory endings. Most of the GTO are not found in the tendon but rather at the transition from tendons to muscle fibers and aponeurotic sheaths. In the cat, there are about 10 muscle fibers in series with a single tendon organ. A contraction of any one of these 10 fibers is sufficient to elicit a discharge in the Ib afferent arising from a GTO.

Basically, the GTO acts as a strain gauge measuring active and passive forces, especially those produced by the inserting muscle fibers (43, 302, 314, 320, and 514 for review). In some instances, it was possible to measure the discharges of all Ib afferent fibers of a single muscle (300). From this study, it appears that tendon organs are very good in following variations in force, and it was concluded that they code for dynamic and not for static muscle force. Initially, it was thought that strong muscle stretch was the optimum stimulus for Golgi tendon afferents (307). However, in the 1960s, it was discovered that small twitches of soleus (320) or tibialis anterior (3) were very effective in eliciting responses from Ib afferents from these muscles. The most convincing evidence for the very high sensitivity to muscle force came from experiments in which stimulation of ventral roots demonstrated that isolated Ib afferents had a very low threshold (1 mN) for their responses to muscle contraction (302). Only under some circumstances the Ib afferents can also effectively be activated by passive stretch. Stuart et al. (512), for example, showed that the firing threshold of tendon organs can be about equal for passive stretch and graded contraction. In most instances, however, passive stretch was clearly less effective than active contraction (440, 509). To validate the role of GTO in measuring muscle force in the intact cat or even in human subjects, one can measure the tendon force directly, using a "buckle" type of tendon transducer as introduced by Yager (540) and used by Walmsley et al. (524) and others (for review, see Ref. 363, 433).

In summary, both in invertebrates and vertebrates (including humans), load receptors can be divided into two groups, namely, main receptors and accessory ones (Table 1). In general, the latter are more sensitive to movement or position than to the load. However, in some particular circumstances, the accessory receptors are sensitive to the load supported. Considering the main receptors, it is also obvious that they are not only detecting load but also muscle tension. In both groups, it seems that the main factor for load recording is the particular location of the receptors in the animal or human. For this reason, the cutaneous afferents from the sole of the feet or the cuticular receptors of the insect leg tarsus or of the crustacean leg dactyl are of primary importance. Although load receptors show many similarities between invertebrates and vertebrates, some major differences exist as well. First, in the arthropods, the presence of an exoskeleton offers some interesting possibilities for recording load by receptors inserted on certain parts of cuticle. This particular material has itself some specific load-resisting properties that have been studied in detail (problem of compliance, see Ref. 23). Second, the ensemble of receptors is much more diverse in invertebrates, ranging from very simple forms (hairs, setae) to complex organizations (cuticular structures, tendon organs). In comparison, in mammals we have mostly rather complex structures (GTO, skin mechanoreceptors).

	V. CONTROL MECHANISMS IN STATIC CONDITIONS

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The aim of this section is to describe direct load feedback through reflexes under static postural conditions. It is realized that there is also an indirect role of load feedback, needed to update internal models used in feedforward control, but this type of feedback mechanism is beyond the scope of this review (see Ref. 136).

A.  Invertebrates

1.  Compensatory movements and righting responses

Load exerted on an animal is one major element to be controlled by equilibrium reactions. The latter can be divided into compensatory movements, when a constant position has to be maintained, and righting responses, in which the appendages actively restore the previous position. In crustaceans, such reactions involve the receptors described previously (cuticular receptors, CO, and the statocysts). The manner in which visual, gravitational, and proprioceptive cues interact in the control of compensatory eye movements has been investigated by Neil (394). Righting reactions are mostly dynamic and involve the generation of forces to oppose external disturbances. The ensuing reaction has then to be integrated in the animal's usual behavioral posture. For example, in Homarus, the elevation of the claw, unilateral swimmeret beating, and uropod opening and closing along with movements of antennae are all motor reactions that are aimed at restoring the upright position (42). Both the statocyst and some proprioceptors have been shown to be important for these reactions. For example, the role of the coxobasal CO has been demonstrated both for the righting reaction of the antennae (102) and for the control of swimmeret beating (84).

In normal stance, arthropods maintain a low center of gravity. As a result, the different leg joints are partially or totally held in a flexed position while head, thorax, and abdomen are held in suspension from the proximal leg joints. Resistance reflexes then ensure the appropriate maintenance of this posture. This includes equilibrium reactions and adjustment of body height.

In the hermit crab, the stabilization of the abdomen has been studied in detail by Chapple (88). A cocontraction reflex is described that is activated by both stretch and release of the central superficial muscles in the abdomen. The reflex has two components and is very sensitive to ramp stretch. It is primarily sensitive to stretch velocity. Mechanoreceptors that produce this response are activated by active force as well as stretch, suggesting closed loop control.

In general, posture is maintained actively by negative feedback produced continuously by sensory afferents controlling the different leg joints in Crustacea as in Insecta depending on the muscles involved in counteracting the gravitational forces. Skorupski et al. (501) demonstrated that a particular pool of MN is devoted to negative feedback, whereas another, more directly connected with central drive, is involved in positive feedback.

The extensor muscles develop the force required for jumping. A special mechanical arrangement within the femur-tibia joint allows a high force to be developed by the extensor muscle, although the joint remains flexed as long as the jump is not yet elicited. During static conditions this flexor force is developed against a cuticular structure and can easily counteract the extensor contraction (while inhibition of this flexor force leads to a jump; see sect. VA2).

Many resistance reflexes are known in arthropods. These are based on position sensors (30, 69, 92, 217). In many cases, where whole joints rather than individual sense organs are stimulated, the participation of load sensors cannot be excluded. By specific stimulation of the CS at the cockroach tibia (551, 553, 554), different reflexes could be induced: proximal sensillae inhibit flexor MN and excite extensor MN, distal sensilla induce opposite responses with excitation of the flexor MN and inhibition of the extensor MN. Such reflexes thus provide negative feedback, since loading the upright standing animal stresses the proximal sensilla, which reflexly excite extensors. Inversely, lifting the animal produces strain in the distal sensilla, thereby causing flexor activation. Therefore, bending of the tibia in either direction is minimized. This corresponds to a load compensation system based on counteracting the bending forces produced by the animal's weight on the leg. In the stick insect, Schmitz (466) confirmed these previous data for a proximal joint that acts perpendicularly to the femur-tibia joint. He studied the role of the trochanteral CS in controlling the retractor and protractor coxal MN. These reflexes also represent a negative feedback system that continuously compensates cuticular stress in the legs of the standing animal. Moreover, he was able to show that these reflexes are also active in the walking animal. During the stance, depending on whether the femur is loaded (in posterior direction) or unloaded, either the retractor coxae or the protractor coxae is excited reflexively. This would lead to a prolongation of the ongoing stance or would facilitate the transition from stance to swing, respectively.

Similarly, in the crayfish, reflexes induced by the CSD receptors have been studied by intracellular recording of different MN. Monosynaptic connections have been found from CSD1 and CSD2 to the different levator and depressor MN, although responses are quite complex and are in the main polysynaptic (352). It may be concluded that during stance, these receptors elicit activity that reflexly induces cocontraction of opposite muscles, which should result in an overall stiffening of the leg. The outcome of the reflexes of CSD1 reflexes depends on the force level (351). Inhibitory responses in the anterior levator were correlated with the activation of low-threshold CSD1 units, and excitatory responses with the activation of high-threshold CSD1 units. For the FCO, the final outcome of the reflexes is totally different. In studies on the crab, rock lobster, and crayfish, stimulation of the FCO dactyl nerve resulted in polysynaptic responses in proximal MN (levator, depressor, promotor, and remotor, Ref. 98). The main response is facilitatory for the levator MN and inhibitory for the depressor MN, thereby causing a limb swing movement.

In crabs, the great sensitivity of tendon receptors to centrally initiated increases in muscle tension suggests that these receptors are very well situated to evoke compensatory motor discharge that will overcome load encountered during leg movements. Stimulation of the tendon receptor nerve inhibits resistance reflex motoneuronal activity in the homonymous muscle and causes some inhibition in the opposing muscle (100). However, depending on the intensity of the stimulation of that nerve, some authors (408) have found some local facilitation, inducing an assisting effect. These receptors then influence the general control of leg joint position and movement (367).

A great variety of reflexes have been described in postural reactions, and all of them involved the load supported by the animal. They can be summarized as resistance reflexes that can be understood as representing negative-feedback controllers. These reflexes counteract the effects of external forces applied to the body. The most important natural case is gravity, which can act in different directions depending on the position of the body, e.g., standing on a vertical plane or hanging upside down from a horizontal beam (stick insect, Ref. 120; cockroach, Ref. 346).

These resistance reflexes and the sense organs responsible for them were investigated in detail for the stick insect (24, 463-465, 527). The whole leg was shown to act as a height controller, and the different legs act independently of each other (standing insect, Refs. 144, 527; walking insect, Refs. 121, 148). It could be shown that the reaction of the whole leg represents mostly, but not completely, the vectorial sum of the resistance reactions of the individual joints (135). Distributed reflexes that might be responsible for these differences were described for crustaceans (92). The resistance reflexes in the individual joints act together to give the leg a springlike behavior.

In the stick insect, the height controller has a dynamic component that adapts to long-term external loads. This results from the sensitivity of the reflexes to extremely slow movements, which is also responsible for the behavior of flexibilitas cerea (32), where a leg after a disturbance seems to remain in that new position. However, in effect, the leg moves back to its original position, but so slowly that is is often very difficult to recognize the movement by eye. As mentioned in section VIIA, the dynamic behavior of the height controllers changes when the animal changes its state from standing to walking; the "spring" now shows a tonic behavior with a small time constant (148, 463).

In spiders, stimulation of tactile hairs on the ventral, proximal part of the legs induced a contraction in some leg muscles that raised the body (204). Such a reaction, which involves coordination of more or less all eight legs, can be induced by stimulation of just one tactile hair with a latency to 100-160 ms. These "tactile hairs" appear to be mechanical touch receptors and are innervated by three bipolar sensory cells. Local IN could suffice to mediate local interleg reflexes, whereas plurisegmental IN may serve to generalize the reaction (380). Several parallel reports have been presented in insects (424, 492).

Some experiments on postural control before jumping in locusts by Burrows and Pflügers (70) have shown positive-feedback effects that could be important in increasing force (and load). The tibia of the hindlegs of the locust is of particular interest because these legs are used in walking, climbing, and providing propulsive force for jumping. The tibia is moved by a powerful extensor muscle and by a much weaker flexor muscle. They alternate during walking but cocontract to generate the high forces required for kicking and jumping. Such force can be measured by two CS disposed in the proximal part of the tibia, one anterior and one posterior; they are excited by strains set up when the tibiae try to extend against a resistance. The afferents excite both flexor and extensor muscles: they excite the fast axon to the extensor (FETI), certain flexor MN, and some nonspiking IN and then indirectly the slow axon to the extensor (SETI). This reflex may be useful during jumping. Before a jump can occur, both flexor and extensor muscles must cocontract, and it is the inhibition of the flexor MN that allows the stored force to be released explosively (286, 287). During the cocontraction, the CS produce afferent spikes so that they contribute to the facilitation of both muscles. Campaniform sensilla appear to make direct connections with the fast extensor; however, there is also an inhibitory influence onto the flexor, and as only the connectivity has been investigated, the functional contribution is still open. Femoral chordotonal afferents also synapse monosynaptically on such MN and on nonspiking IN, spiking local IN and intersegmental IN. Inhibition of flexion originates from the IN, which can be gradually depolarized and which inhibit the flexor directly (67).

The role of sensory feedback in postural control has been the subject of several reviews (162, 272, 371, 372). Here we focus on the issue of load-compensating reflexes.

It has been difficult to assess the reflex effects from Ib afferents because few methods are available to activate these afferents in isolation reliably. Most of the early studies (202, 203, 345) used electrical stimulation of nerves to study the reflex responses in cats. The main problem, however, is that Ia and Ib fibers have about the same diameter, and it is usually impossible to selectively activate the Ib afferents. For a few nerves, such as the ones innervating knee flexors and extensors, one can activate Ia afferents before reaching the Ib threshold (46), and this feature was extensively used to separate Ia from Ib effects (see Ref. 374 for review).

On the basis of these studies, it was first concluded that Ib afferent activity induced inhibition in the MN of homonymous muscles, while providing excitation to antagonist MN ("the inverse myotatic reflex," Ref. 345). It soon became clear that this was a misleading term, since the projections were much more widespread, and there was no distinct inhibition favoring the parent muscle (202, 203). In fact, the effects were present even in muscles acting across different joints. Sometimes the effects were opposite: Ib afferent input from extensors causing inhibition of flexors (202, 203). The latter type of "exception" was found quite often when the Ib reflex effects were studied during facilitations from some descending tracts (rubrospinal tract, Ref. 298). Furthermore, studies using spike-triggered averaging showed that Ib effects were frequently excitatory to synergistic MN (525).

More recently, large changes in gain of Ib reflexes have been demonstrated by les