J Appl Physiol 96: 1961-1967, 2004;
doi:10.1152/japplphysiol.01073.2003
8750-7587/04 $5.00
INVITED REVIEW
HIGHLIGHTED TOPICS
Neural Control of Movement
Sensorimotor integration at spinal level as a basis for muscle coordination during voluntary movement in humans
Jens Bo Nielsen
Institute of Physical Exercise and Sport Science and Department of Medical Physiology, The Panum Institute, University of Copenhagen, 2200 Copenhagen, Denmark
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ABSTRACT
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Spinal reflexes have traditionally been treated as separate from voluntary movements. However, animal experiments since the 1950s and human experiments since the 1970s have documented that sensory activities in afferents from muscles, skin, and joints are integrated with descending motor commands at the level of common spinal interneurons. Two different roles of this sensorimotor integration at the spinal level may be discerned. First, sensory feedback evoked by the active muscles may help to drive the motoneurons. Second, external stimuli, such as sudden perturbations of a limb, may give rise to "error signals," which are integrated into the ongoing motor activity and form the basis of corrective responses. When interpreting experimental data, it is important to consider these two different roles. Application of external stimuli may provide little information about how the spinal cord integrates sensory feedback evoked as part of ongoing movements. The complexity of the spinal machinery that is activated by external stimuli also makes the interpretation of data obtained from experiments dealing with artificial external stimuli, such as electrical stimuli, difficult. Nevertheless, such experiments have provided and will continue to provide very valuable information about how the brain and spinal cord ensure coordination of muscle activity during voluntary movement. So far, spinal control mechanisms have only been investigated to a limited extent in relation to sports and occupational activities. Provided that researchers consider the methodological problems of the techniques and that they seek independent validation of the findings, this may be a very fruitful research field in the future.
central motor commands; sensory afferents; applied motor control; spinal cord
IT HAS BEEN ACCEPTED FOR A long time that integration of sensory feedback signals and central motor commands at several levels of the central nervous system plays a pivotal role in controlling our movements. At the spinal level, research on the cat spinal cord since the 1950s has documented that sensory afferents and descending motor pathways converge onto common spinal interneurons (reviewed in Ref. 1; see also Ref. 19a). Subsequent human studies since the 1970s have documented how this integration of motor commands and sensory feedback signals is used to control muscle activity during movements. The information arising from this research is of obvious importance in relation to sports and occupational activities; however, this type of research has only been applied to a very limited extent to the type of movements encountered in such activities and is not well represented in journals devoted to applied motor control. With this review, I hope to stir the interest for using noninvasive electrophysiological techniques in combination with biomechanical and kinematic techniques in the field of applied motor control.
I do not intend to provide a comprehensive review of the field but rather to discuss some issues that I find fundamental for understanding the way that the spinal cord machinery is used by the brain to control movement. I will make three different points in the paper. 1) There has been a lot of discussion on the functional role of reflexes over the years, but reflexes are usually not evoked in isolation during normal conditions in human subjects. The sensory feedback and the activity in the spinal pathways evoked by this activity are rather an integrated part of the central motor command reaching the muscles during voluntary movements. 2) The often-used distinction between open-loop control (without sensory feedback) and closed-loop control (with sensory feedback) is artificial. Sensory feedback and lack of sensory feedback are both important sources of information for the brain and spinal cord; in predicted, unperturbed movements, both are integrated parts of the central motor command to the muscle. When perturbations occur, increased and decreased sensory feedbacks act as valuable error signals to the brain. 3) If we are to understand the fundamental principles of sensorimotor interaction at a spinal level and the significance of this interaction for the execution of functional motor tasks, we need to perform more experiments, combining electrophysiological evaluation of the transmission in identified spinal pathways with precise biomechanical and kinematic analyses of the exerted movements.
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STUDYING THE ROLE OF SPINAL INTERNEURONS IN THE CONTROL OF MOVEMENT
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Around 50 years of experimental animal research have resulted in a detailed account of the complex organization of the cat lumbar spinal cord (1, 19a). Although this research has been very powerful in identifying and characterizing the interneuronal populations in terms of their input and output organization, it has been far less powerful in demonstrating the functional role of the interneuronal populations in relation to movements. This is an inherent consequence of the experimental approach, which usually requires the animal to be either anesthetized or decerebrated. In only a few studies have direct recordings of the activity of the spinal interneurons been attempted in relation to actual motor behavior. This is partly because of the technical difficulties in obtaining stable recordings during movements and partly because of the difficulties in identifying the interneurons in the intact behaving animal. Recent chronic recordings of interneurons in the monkey cervical spinal cord (25, 36) have made an important step in the right direction; however, full identification of the interneurons is not yet technically possible, which limits the interpretation of the data. Recordings of the discharge of identified interneurons in the cat lumbar spinal cord during fictive locomotion are also of great interest (40), but the removal of both supraspinal and peripheral sensory input to the interneuronal populations questions the general applicability of the findings.
For these reasons, it is important that noninvasive techniques have become available through indirect evidence of the activity of identified spinal interneuronal populations during movements in awake human subjects may be obtained.
It was the demonstration of disynaptic reciprocal Ia inhibition in human subjects and its modulation during voluntary movement by Tanaka in 1974 (45) that stirred the interest of researchers and opened the field (although partly similar findings had been published earlier; see Refs. 22 and 28). Because the disynaptic reciprocal inhibitory pathway involves only a single interneuron and is highly characteristic by its reciprocal organization, it still represents the most ideal illustration of the way that noninvasive techniques may be used to study the control of spinal interneuronal pathways during movement. Figure 1 illustrates how disynaptic reciprocal inhibition may be demonstrated directly in the cat (A and B) and more indirectly by noninvasive techniques in human subjects (C and D). In the cat, it is possible to record simultaneously from the interneurons in the pathway and the motoneurons to which they project. When group Ia afferents are stimulated, disynaptic inhibition is produced in the motoneurons of its antagonists (Fig. 1B). The interneurons in the pathway may be identified by the monosynaptic excitatory postsynaptic potential produced by the Ia stimulation and the inhibitory postsynaptic potential (IPSP) produced in the target motoneurons by their discharge (Fig. 1B; in addition, the interneurons are also characterized by the existence of inhibition from Renshaw cells).
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Fig. 1. Demonstration of the disynaptic reciprocal Ia inhibitory pathway in the cat (A and B) and in humans (C and D). Electrical stimulation of a motor nerve elicits disynaptic inhibitory postsynaptic potentials (IPSPs) in motoneurons of the antagonist muscles. Ia inhibitory interneurons (int), which convey this reciprocal inhibition, are identified in the cat spinal cord by demonstration of monosynaptic excitatory potentials (EPSPs) in intracellular recordings from the interneurons subsequent to motor nerve stimulation [quadriceps (Q) in the illustrated example]. Further identification is obtained by demonstration of recurrent inhibition evoked by stimulation of the corresponding ventral roots (VR; A). B, bottom: monosynaptic EPSP recording from an interneuron. B, top: recording from the cord dorsum. The projection of the interneurons may be demonstrated by the appearance of unitary IPSPs in intracellular recordings from target motoneurons [posterior biceps-semitendinosus (Pbst) motoneurons in the illustrated example] time locked to discharges of the interneurons (B). In human subjects (C and D), transmission in the disynaptic Ia inhibitory pathway may be demonstrated indirectly by the H-reflex technique. The H reflex is influenced by changes in the excitability of the spinal motoneurons. If a disynaptic IPSP is therefore elicited by stimulation of a motor nerve [in the illustrated example, the peroneal nerve (PN) was stimulated], the transient hyperpolarization of the motoneurons (soleus motoneurons in the illustrated example) will result in a decrease in the size of the H reflex. This is illustrated in D, top. The soleus H reflex was depressed to  70% of its control size when the stimulation of the PN was applied 2 ms before stimulation of the tibial nerve (TN), which elicited the H reflex. This fits well with transmission in a disynaptic pathway, since the 2 stimulations were applied at roughly the same distance from the spinal cord and since the involved afferents have roughly the same conduction velocity. That Ia afferents are the likely cause of the inhibition is evidenced by the very low threshold at which it is seen (D, bottom). Mmax, maximal M response; Cond, conditioning.
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A similar direct demonstration of disynaptic reciprocal inhibition is naturally not possible in human subjects. However, in human subjects, the inhibition may be demonstrated as a decreased excitability of the spinal motoneurons shortly after the stimulation of the antagonist group Ia afferents. This is illustrated in Fig. 1, C and D. Stimulation of a peripheral nerve (e.g., the tibial nerve) will activate group Ia afferents, which have monosynaptic projections to the spinal motoneurons innervating the same muscle (e.g., the soleus muscle). The stimulation will therefore result in a reflex discharge, which may be recorded in the EMG from the muscle. This reflex is the so-called Hoffmann or H reflex (named after the German neurologist Poul Hoffmann, who described it in 1918), and its size is determined primarily by the amount of transmitter release from the Ia afferents and the excitability of the spinal motoneurons. If the excitability of the spinal motoneurons is therefore decreased by an IPSP elicited by activation of the reciprocal inhibitory pathway, this will be seen as a decrease in the size of the H reflex. In accordance with this, activation of the disynaptic reciprocal inhibitory pathway by stimulation of group Ia afferents from the ankle dorsiflexors depresses the soleus H reflex at a very short latency (Fig. 1C). Both the latency and the low threshold of the inhibition suggest that it is mediated by the reciprocal disynaptic group Ia inhibitory pathway.
Tanaka (45) demonstrated that the inhibition of the soleus H reflex from stimulation of the peroneal nerve became larger when the subjects voluntarily activated the ankle dorsiflexor muscles. In cat, monkey, and human subjects, descending motor pathways have been shown to project in parallel to the spinal motoneurons and the reciprocal Ia inhibitory interneurons projecting to the antagonist motoneurons (19, 20, 24, 35). The most straightforward explanation of Tanaka's finding was that the transmission in the pathway was facilitated by the voluntary motor command to the ankle dorsiflexors through the parallel activation of spinal motoneurons and interneurons. Tanaka did not take into account that the sensitivity of the H reflex to inhibitory influences depends on its size (6, 7); therefore, much of the apparent increase of inhibition that he observed during dorsiflexion may be explained by the smaller reflexes in that situation compared with at rest (5, 6). Nevertheless, subsequent experiments have confirmed that disynaptic reciprocal inhibition to ankle plantar flexors is indeed increased in relation to at least the dynamic part of a voluntary ankle dorsiflexion (Fig. 2A) and that this is caused by supraspinal influences, since a similar facilitation of the transmission in the pathway may be seen when afferent feedback from the active dorsiflexor muscles is blocked by ischemia or injection of a local anesthetic (30, 34). Facilitation of transmission in the pathway may also be observed before the onset of movement (6). The reciprocal nature of this control has also been demonstrated by the decreased disynaptic reciprocal inhibition to ankle plantar flexors during activation of these muscles (Refs. 6 and 18; Fig. 2B) and opposite changes for the pathway from ankle plantar flexors to ankle dorsiflexors (6, 31). These findings and those of several other findings for other muscles (10) and other types of movements, including walking and bicycling (37, 41), have led to the present view on the control and functional significance of disynaptic Ia reciprocal inhibition (Fig. 3). During voluntary movement, disynaptic reciprocal inhibition of the antagonist muscles is increased to ensure that these remain silent during the movement and that no unwanted stretch reflex activity is evoked; disynaptic reciprocal inhibition onto the active muscle, however, is decreased to facilitate the activation of that muscle.
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Fig. 2. Supraspinal modulation of transmission in the disynaptic reciprocal inhibition in relation to ankle plantar flexion (A) and dorsiflexion (B) in humans. Disynaptic reciprocal inhibition of the soleus H reflex (Sol H) was evoked by stimulation of the PN in the same way as in Fig. 1, C and D. The conditioning-test interval between PN stimulation and TN stimulation was 2 ms throughout the experiment, i.e., at an interval at which the maximal amount of inhibition was seen (see Fig. 1D, top). PN stimulation was maintained at 1.05 x motor threshold, and a small M response was monitored in the tibialis anterior muscle to ensure that the stimulation conditions were stable. The size of the control H reflex was maintained at a size 20% of the maximal M response throughout the experiment. The subject's task was to perform an isometric ramp-and-hold plantar flexion or dorsiflexion. The ramp phase lasted 300 ms, whereas the hold phase lasted 1 s. Contractions were repeated every 10 s. The disynaptic reciprocal inhibition decreased considerably already before the onset of EMG in the soleus muscle in relation to plantar flexion and was smaller than at rest throughout the ramp phase of the contraction. Conversely, in relation to dorsiflexion, a significant increase of the inhibition was seen before the onset of EMG in the ankle dorsiflexors, and this increase of inhibition was maintained throughout the ramp phase of the contraction. Because these changes were observed before any changes in EMG activity, they must be caused by supraspinal control of the transmission in the Ia inhibitory pathway. Both the removal of inhibition of the motoneurons that are going to be activated (i.e., reduced inhibition in relation to plantar flexion) and the increased inhibition of the antagonist motoneurons that would counteract the movement (i.e., the increased inhibition in relation to dorsiflexion) make good functional sense. CPN, common peroneal nerve.
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Fig. 3. Parallel control of spinal motoneurons and corresponding Ia inhibitory interneurons. Cat, monkey, and human experiments have documented that Ia afferents and descending supraspinal pathways project in parallel to spinal motoneurons and their corresponding Ia inhibitory interneurons. This makes the basis for the observations in Fig. 2. In relation to dorsiflexion, the Ia inhibitory interneurons projecting to soleus motoneurons are thus facilitated by collaterals from the descending projections to the tibialis anterior motoneurons. Conversely, in relation to plantar flexion, the Ia inhibitory interneurons projecting to ankle dorsiflexor motoneurons are facilitated by collaterals of descending projections to plantar flexor motoneurons. Because these interneurons also project to the Ia inhibitory interneurons, which project in the opposite direction (i.e., from ankle dorsiflexors to plantar flexors), this explains the decrease of inhibition observed in relation to plantar flexion in Fig. 2.
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Although experiments in the cat had certainly pointed in the same direction, based on observations of the parallel sensory and supraspinal projections to spinal motoneurons and Ia inhibitory interneurons, these experiments were not able to make as conclusive a demonstration as for the human experiments. In fact, it is only after the publication of the initial human studies that experiments during fictive locomotion demonstrated that Ia inhibitory interneurons display similar alternating activity patterns, as suggested by human studies (40). In addition, several other pathways contribute to the inactivation of antagonistic muscles during movement (8). However, the disynaptic reciprocal Ia inhibition is the best-studied and best-understood mechanism.
During the past 20 years, numerous studies have used the same fundamental technique as described for disynaptic reciprocal inhibition to study the supraspinal control of transmission in other spinal pathways, including autogenic Ib inhibition (14), recurrent inhibition (38), group II pathways (27), and presynaptic inhibition (8, 17, 33). It is outside the scope of this mini-review to describe all the various interneuronal populations and pathways and discuss their functional significance in relation to voluntary movement. For more information about the various interneuronal populations, the reader may consult the review by Baldissera et al. (1) as well as the monographs by Rothwell (42) and Porter and Lemon (39).
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METHODOLOGICAL PROBLEMS
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The research described above has been followed by a continuous criticism of the techniques, leading to improvements and refinements of the existing techniques as well as the development of new supplementing techniques. The importance of maintaining a comparable control reflex size when comparing two different situations as illustrated by Tanaka's findings (45) in relation to disynaptic reciprocal Ia inhibition during dorsiflexion is only one example of methodological problems that have been clarified and resulted in improved techniques. Other important methodological problems include the following: 1) activity in Ia afferents may lead to prolonged changes in the transmitter release from their synapses (postactivation depression), which may interfere with the determination of the size of both inhibitory and excitatory effects on the H reflex (9, 16); 2) the gain with which the H reflex recruits motoneurons may change during different tasks, which will also interfere with the determination of inhibitory and excitatory effects (21, 33); 3) the H reflex may not be fully monosynaptic but may be influenced to a varying extent by transmission in nonmonosynaptic pathways (2, 26), which may confound the interpretation of the data. All of these problems may be related to the fact that the H reflex measures the effect of activation of a pool of motoneurons. It is therefore generally recommended to confirm findings with the H reflex technique by an independent technique. One such technique is the poststimulus time histogram technique, which may be used to investigate the effect of activation of a spinal pathway on a single motoneuron. In this technique, the discharge probability of a single motor unit is recorded with and without activation of a specific pathway. Increases or decreases in the discharge probability of the unit at specific time lags after the activation of the pathway will then reflect excitatory or inhibitory influences on the motoneuron, and the size of these effects will reflect the transmission through the pathway. When comparing two different situations in which the motor unit is active, information about changes in the transmission in the pathway may thereby be obtained. If data obtained with the H reflex and poststimulus time histogram techniques point in the same direction, the conclusions may be reached on a much more solid ground than if only data from one of the techniques were obtained.
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SHOULD WE CALL IT SENSORY FEEDBACK CONTRIBUTION TO CONTROL OF MOVEMENT RATHER THAN REFLEXES?
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The functional role of each of the various populations of spinal interneurons is different, and their study generally tells us something new about sensorimotor interaction at the spinal level. General conclusions regarding the role of sensorimotor interaction at a spinal level are therefore difficult to make. In the following, I will, however, discuss some topics that are of general relevance for sensorimotor interaction at the spinal level.
Research in both animal and human subjects has shown that convergence between descending supraspinal input and sensory feedback on common spinal interneurons is a cornerstone in the central control of movement. Although the neuronal circuits in the spinal cord certainly may give rise to reflex activity following an adequate stimulus, it should be emphasized that this is not the normal function of the pathways during normal behavior in intact humans. The separation of "spinal reflexes" and "voluntary movement" in separate chapters in many textbooks (Fig. 4A) is not justified based on the present knowledge and understanding of the way that the spinal interneuronal network is organized and functions. It would be more adequate if emphasis was placed on how sensory feedback in specific spinal interneuronal pathways contributes to the activation of the muscles and to their inactivation, when this is required (Fig. 4B). The reflexes certainly have a specific function in primitive invertebrate animals; however, in more complex animals such as humans, it is not possible to discuss in a meaningful way the functional significance of a reflex without considering its integration with the supraspinal motor commands underlying voluntary movements.
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Fig. 4. Two different views of the organization of reflexes and voluntary movements. In older literature and in many modern textbooks, reflexes and voluntary movements are treated as separate entities (A). In fact, as shown in Figs. 1 and 2, reflexes and voluntary movements are inseparable because sensory afferents and descending supraspinal pathways converge on the same interneurons (B). Rather than a discussion of the functional significance of reflexes, which is quite common in many publications, it is more reasonable to discuss the role of sensory modulation of the voluntary movements.
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SENSORY FEEDBACK CONTRIBUTION TO ONGOING MUSCLE ACTIVITY AND SENSORY FEEDBACK AS AN ERROR SIGNAL
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It is important to make a distinction between the sensory activity that is evoked as part of a preprogrammed movement and the sensory activity that is evoked by a sudden, unexpected perturbation of the movement or activation of a sensory receptive field. In the former case, the sensory activity is anticipated by the central nervous system, and it is an essential integrated part of the central motor command reaching the muscles. In the latter case, the sensory activity is an error signal, informing the central nervous system that the movement was not performed according to the plan or that an obstacle was met. In reality, a completely clear distinction between these two modes of sensory feedback does not exist, since the sensory activity evoked during a movement probably never fully corresponds to that expected and therefore could be said also to contain some "error signal." Such error signals probably help to update the brain and optimize the motor program during movements. Nevertheless, there is at least a quantitative difference between such small deviations from the expected feedback and the much larger deviations evoked by external stimuli.
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SENSORY FEEDBACK MECHANISMS CONTRIBUTE TO THE ACTIVATION OF THE MUSCLES DURING ONGOING MOVEMENTS
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The evidence that sensory feedback contributes significantly to the muscle activity during movement comes from studies in both the cat and human subjects (35a, 44). In the stance phase of walking, muscle spindle afferents and force-sensitive afferents discharge due to increased gamma drive and increased muscle load, respectively. If this sensory afferent feedback contributes to the activation of the muscles, a sudden drop in activity should result in a decrement in the EMG activity recorded from the active muscles. This was also what Sinkjær et al. (44) observed when the ankle plantar flexor muscles were suddenly unloaded in the middle of the stance phase. The unload was performed by a portable mechanical device, which could suddenly superimpose a plantar flexion movement on the ongoing ankle joint trajectory or prevent the ongoing dorsiflexion movement in the middle of stance. In both cases, a very clear drop in the EMG activity recorded from the soleus muscles was observed at a latency of 60 ms after the onset of the unload. Control experiments with local anesthesia were performed to exclude that the observed drop in EMG activity could be caused by activation of afferents from the antagonist muscle, ankle joint afferents, or cutaneous afferents. The study by Sinkjær et al. thus demonstrated that length and/or load-sensitive afferents from the ankle plantar flexors contribute to the activation of the soleus muscle during the stance phase of walking through feedback to spinal interneuronal pathways. Convergence on the interneurons in these pathways from the sensory afferents and descending supraspinal fibers determines the synaptic drive to the spinal motoneurons; thus removal of either one, i.e., by unloading/shortening of the muscle leading to decreased sensory afferent feedback (44) or inhibition of the cortical function by transcranial magnetic stimulation leading to decreased corticospinal drive (36a), results in a significant drop in the muscle activity.
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EXTERNALLY EVOKED CHANGES IN SENSORY FEEDBACK ACT AS ERROR SIGNALS
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Whenever an external stimulus causes the sensory feedback to deviate from that expected by the central motor program, the sensory feedback may serve as an error signal. For example, this occurs when a subject stumbles over an obstacle or when instabilities of the ground lead to perturbation of the supporting foot. In both cases, corrective reactions are elicited at relatively short latency (usually 70-120 ms). It is important to realize that both increased and decreased sensory feedback act as error signals. Lack of sensory feedback in a situation where sensory activity is expected is as much as an error signal as the increased sensory activity caused by stimulation of the sensory receptors. Note that in the study by Sinkjær et al. (44) the normal contribution of the positive feedback mechanism is inferred from the drop in EMG activity caused by the external perturbation. However, the decrease in sensory activity that it reflects acts as an error signal for later corrective reactions.
Responses evoked by activation of sensory receptors in muscles and skin have been studied in a long range of studies during various types of movement (4, 11, 12, 43, 47, 48; see also Ref. 3). Such studies have provided important information about the central modulation of the responses evoked by sudden external perturbations and have helped to emphasize the importance of the sensorimotor interaction in the spinal cord as well as supraspinal sites for the elicitation of appropriate corrective reactions.
It is not straightforward to make inferences about the contribution of sensory activity to the ongoing movement based on such studies. The afferents may not normally be active in the phase where they are activated by the external stimulus (particularly in the case of cutaneous afferents). Observations of a large or small reflex response in that phase of the movement would thus say very little about the normal (unperturbed) function of the afferent feedback. On the other hand, if an external stimulus is applied at a time when the sensory afferents are already very active, the evoked responses may be small instead of large due to occlusion in the pathway. Data from both humans and cats also suggest that the central gating of the desynchronized and relatively low-rate sensory activity, characteristic of the normal afferent feedback and the sudden (artificial) highly synchronized afferent feedback evoked by an external stimulation (13, 29), may be very different.
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SHOULD WE ABANDON THE "CLOSED LOOP-OPEN LOOP" CONCEPT?
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From available data on sensorimotor interaction in the spinal cord, I do not find it reasonable to distinguish between the "open-loop" (without sensory feedback) and "closed-loop" modes of motor control, although this distinction is often advanced in motor control textbooks. Sensory feedback is manifest already 50 ms after the onset of movement (46), and no movements are therefore so quick that they can be executed before sensory feedback has reached the spinal cord. Even if it is granted that the first 50 ms of all movements have to be performed in an open-loop mode, my point is that the sensory feedback, which occurs at 50 ms after onset of movement (and later), is "anticipated" by the central nervous system and "builds" into the central motor program. Furthermore, even in the resting situation, sensory feedback is constantly informing the central nervous system about the position of joints and limbs; this information is necessary for the central nervous system to ensure the correct movement of a limb from one position to another. The loop is thus in reality not "open."
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FUNCTIONAL RELEVANCE OF DATA OBTAINED BY NONINVASIVE ELECTROPHYSIOLOGICAL EXPERIMENTS IN HUMANS
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Electrophysiological experiments such as those described in this mini-review have only to a limited extent been applied to functional every-day motor tasks; in many studies, only a rather rudimentary biomechanical or kinematic analysis of the exerted movement has been performed. This is because these studies have focused on characterizing and defining the central pathways under study rather than making any functional deductions. This is in stark contrast to the majority of research on applied motor control, which focus on functional application and in which detailed biomechanical and kinematic analyses of the movement are the rule. The drawback of these latter studies is that there is very little chance that phenomenological descriptions on their own will provide us with any fundamental understanding of how movements are initiated and controlled, how the execution of movement is optimized, and what goes wrong when movements fail to reach their goal. Clearly, there is a great need that the "neurophysiological tradition" and the "biomechanical/kinematic tradition" are combined. Such a combined approach has the potential of providing us with a fundamental understanding of the functional outcome of sensory-motor integration in identified spinal pathways, and it may help us to understand how the central nervous system controls the types of movements involved in sports and occupational activities.
I hope with this mini-review to have stirred the interest for performing such experiments.
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FOOTNOTES
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Address for reprint requests and other correspondence: J. B. Nielsen, Institute of Physical Exercise and Sport Science and Dept. of Medical Physiology, The Panum Institute, Copenhagen Univ., Blegdamsvej 3, 2200 Copenhagen N., Denmark (E-mail: J.B.Nielsen{at}mfi.ku.dk).
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REFERENCES
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- Baldissera F, Hultborn H, and Illert M. Integration in spinal neuronal systems. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Soc., 1981, sect. 1, vol. II, pt. I, chapt. 12, p. 509-595.
- Burke D, Gandevia SC, and McKeon B. Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J Neurophysiol 52: 435-448, 1984.[Abstract/Free Full Text]
- Capaday C. The special nature of human walking and its neural control. Trends Neurosci 25: 370-376, 2002.[CrossRef][ISI][Medline]
- Capaday C and Stein RB. Amplitude modulation of the soleus H-reflex in the human during walking and standing. J Neurosci 6: 1308-1313, 1986.[Abstract]
- Crone C, Hultborn H, and Jespersen B. Reciprocal Ia inhibition from the peroneal nerve to soleus motoneurones with special reference to the size of the test reflex. Exp Brain Res 59: 418-422, 1985.[ISI][Medline]
- Crone C, Hultborn H, Jespersen B, and Nielsen J. Reciprocal Ia inhibition between ankle flexors and extensors in man. J Physiol 389: 163-185, 1987.[Abstract/Free Full Text]
- Crone C, Hultborn H, Mazieres L, Morin C, Nielsen J, and Pierrot-Deseilligny E. Sensitivity of monosynaptic test reflexes to facilitation and inhibition as a function of the test reflex size: a study in man and the cat. Exp Brain Res 81: 35-45, 1990.[ISI][Medline]
- Crone C and Nielsen J. Methodological implications of the post-activation depression. Exp Brain Res 78: 28-32, 1989.[ISI][Medline]
- Crone C and Nielsen J. Spinal mechanisms in man contributing to reciprocal inhibition during voluntary dorsiflexion of the foot. J Physiol 416: 255-272, 1989.[Abstract/Free Full Text]
- Day BL, Marsden CD, Obeso JA, and Rothwell JC. Reciprocal inhibition between the muscles of the human forearm. J Physiol 349: 519-534, 1984.[Abstract/Free Full Text]
- Dietz V, Quintern J, and Berger W. Corrective reactions to stumbling in man: functional significance of spinal and transcortical reflexes. Neurosci Lett 44: 131-135, 1984.[CrossRef][ISI][Medline]
- Duysens J, Trippel M, Horstmann GA, and Dietz V. Gating and reversal of reflexes in ankle muscles during human walking. Exp Brain Res 82: 351-358, 1990.[ISI][Medline]
- Enríquez-Denton M, Morita H, Christensen LOD, Petersen N, Sinkjaer T, and Nielsen JB. Interaction between peripheral afferent activity and presynaptic of Ia afferents in the cat. J Neurophysiol 88: 1664-1674, 2002.[Abstract/Free Full Text]
- Fournier E, Katz R, and Pierrot-Deseilligny E. Descending control of reflex pathways in the production of voluntary isolated movements in man. Brain Res 288: 375-377, 1983.[CrossRef][ISI][Medline]
- Hoffmann P. über die Beziehungen der Sehnenreflexe zur willkürlichen Bewegung und zum Tonus. Zetischrift Biol 68: 351-370, 1918.
- Hultborn H, Illert M, Nielsen J, Ballegaard M, Paul A, and Wiese H. On the mechanism of the post-activation depression of the H-reflex in human subjects. Exp Brain Res 108: 450-462, 1996.[ISI][Medline]
- Hultborn H, Meunier S, Pierrot-Deseilligny E, and Shindo M. Changes in presynaptic inhibition of Ia fibres at the onset of voluntary contraction in man. J Physiol 389: 757-772, 1987.[Abstract/Free Full Text]
- Iles JF. Reciprocal inhibition during agonist and antagonist contraction. Exp Brain Res 62: 212-214, 1986.[ISI][Medline]
- Iles JF and Pisini JV. Cortical modulation of transmission in spinal reflex pathways of man. J Physiol 455: 425-446, 1992.[Abstract/Free Full Text]
- Jankowska E. Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38: 335-378, 1992.[CrossRef][ISI][Medline]
- Jankowska E, Padel Y, and Tanaka R. Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey. J Physiol 258: 467-487, 1976.[Abstract/Free Full Text]
- Kernell D and Hultborn H. Synaptic effects on recruitment gain: a mechanism of importance for the input-output relations of motoneurone pools? Brain Res 507: 176-179, 1990.[CrossRef][ISI][Medline]
- Kots IM and Zhukov VI. Superspinal control of segmentary centers of muscle-antagonists in man. 3. "Tuning" of a spinal apparatus of reciprocal inhibition during organization of voluntary movement. Biofizika 16: 1085-1089, 1971.[Medline]
- Lemon RN. The GL Brown Prize Lecture. Cortical control of the primate hand. Exp Physiol 78: 263-301, 1993.[ISI][Medline]
- Lundberg A and Voorhoeve PE. Pyramidal activation of various spinal reflex arcs in the cat. Experientia 17: 46-53, 1961.[CrossRef][ISI][Medline]
- Maier MA, Perlmutter SI, and Fetz EE. Response patterns and force relations of monkey spinal interneurons during active wrist movement. J Neurophysiol 80: 2495-2513, 1998.[Abstract/Free Full Text]
- Marchand-Pauvert V, Nicolas G, Burke D, and Pierrot-Deseilligny E. Suppression of the H reflex in humans by disynaptic autogenetic inhibitory pathways activated by the test volley. J Physiol 542: 963-976, 2002.[Abstract/Free Full Text]
- Marchand-Pauvert V, Simonetta-Moreau M, and Pierrot-Deseilligny E. Cortical control of spinal pathways mediating group II excitation to human thigh motoneurones. J Physiol 517: 301-313, 1999.[Abstract/Free Full Text]
- Mizuno Y, Tanaka R, and Yanagisawa N. Reciprocal group I inhibition on triceps surae motoneurons in man. J Neurophysiol 34: 1010-1017, 1971.[Free Full Text]
- Morita H, Petersen N, Christensen LO, Sinkjær T, and Nielsen J. Sensitivity of H-reflexes and stretch reflexes to presynaptic inhibition in man. J Neurophysiol 80: 610-620, 1998.[Abstract/Free Full Text]
- Nielsen J, Crone C, Sinkjaer T, Toft E, and Hultborn H. Central control of reciprocal inhibition during fictive dorsiflexion in man. Exp Brain Res 104: 99-106, 1995.[ISI][Medline]
- Nielsen J and Kagamihara Y. The regulation of disynaptic reciprocal inhibition during cocontraction of antagonistic muscles in man. J Physiol 456: 373-391, 1992.[Abstract/Free Full Text]
- Nielsen J and Kagamihara Y. The regulation of presynaptic inhibition during cocontraction of antagonistic muscles in man. J Physiol 464: 575-593, 1993.[Abstract/Free Full Text]
- Nielsen J and Kagamihara Y. Differential projection of the sural nerve to early and late recruited tibialis anterior motor units: change of the recruitment gain. Acta Physiol Scand 147: 385-401, 1993.[ISI][Medline]
- Nielsen J, Kagamihara Y, Crone C, and Hultborn H. Central facilitation of reciprocal inhibition during tonic dorsiflexion revealed after blockade of peripheral feedback. Exp Brain Res 88: 651-656, 1992.[ISI][Medline]
- Nielsen J, Petersen N, Deuschl G, and Ballegaard M. Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol 471: 223-243, 1993.[Abstract/Free Full Text]
- Pearson KG, Misiaszek JE, and Fouad K. Enhancement and resetting of locomotor activity by muscle afferents. Ann NY Acad Sci 860: 203-215, 1998.[Abstract/Free Full Text]
- Perlmutter SI, Maier MA, and Fetz EE. Activity of spinal interneurons and their effects on forearm muscles during voluntary wrist movements in the monkey. J Neurophysiol 80: 2475-2494, 1998.[Abstract/Free Full Text]
- Petersen NT, Butler JE, Marchand-Pauvert V, Fisher R, Ledebt A, Pyndt HS, Hansen NL, and Nielsen JB. Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking. J Physiol 537: 651-665, 2001.[Abstract/Free Full Text]
- Petersen N, Morita H, and Nielsen J. Modulation of reciprocal inhibition between ankle extensors and flexors during walking in man. J Physiol 520: 605-619, 1999.[Abstract/Free Full Text]
- Pierrot-Deseilligny E, Katz R, and Hultborn H. Functional organization of recurrent inhibition in man: changes preceding and accompanying voluntary movements. Adv Neurol 39: 443-457, 1983.[Medline]
- Porter R and Lemon RN. Corticospinal Function and Voluntary Movement. Oxford, UK: Oxford University Press, 1995, p. 1-448.
- Pratt CA and Jordan LM. Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion. J Neurophysiol 57: 56-71, 1987.[Abstract/Free Full Text]
- Pyndt HS and Nielsen JB. Changes in reciprocal inhibition across the ankle joint with changes in external load and pedaling rate during bicycling. J Neurophysiol 90: 3168-3177, 2003.[Abstract/Free Full Text]
- Rothwell JC. Control of Human Voluntary Movement. London: Croom Helm. 1987, p. 1-350.
- Sinkjær T, Andersen JB, and Larsen B. Soleus stretch reflex modulation during gait in humans. J Neurophysiol 76: 1112-1120, 1996.[Abstract/Free Full Text]
- Sinkjær T, Andersen JB, Ladouceur M, Christensen LOD, and Nielsen JB. Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man. J Physiol 523: 817-827, 2000.[Abstract/Free Full Text]
- Tanaka R. Reciprocal Ia inhibition during voluntary movements in man. Exp Brain Res 21: 529-540, 1974.[ISI][Medline]
- Vallbo AB. Discharge patterns in human muscle spindle afferents during isometric voluntary contractions. Acta Physiol Scand 80: 552-566, 1970.[Medline]
- Yang JF and Stein RB. Phase-dependent reflex reversal in human leg muscles during walking. J Neurophysiol 63: 1109-1117, 1990.[Abstract/Free Full Text]
- Yang JF, Stein RB, and James KB. Contribution of peripheral afferents to the activation of the soleus muscle during walking in humans. Exp Brain Res 87: 679-687, 1991.[ISI][Medline]
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