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Crosstalk opposing view: Independent fusimotor control of muscle spindles in humans: there is little to gain

2021; Wiley; Volume: 599; Issue: 10 Linguagem: Inglês

10.1113/jp281337

1469-7793

David Burke,

Tactile and Sensory Interactions

As envisaged by Paillard (1959), alerting manoeuvres, such as the Jendrassik manoeuvre, potentiate tendon jerks in remote non-contracting muscles due to widespread activation of dynamic γ motoneurons. Paillard's research was ground-breaking, but there are reservations with this hypothesis (Pierrot-Deseilligny & Burke, 2012). It was based on evidence that the H reflex was not potentiated by the manoeuvre. However many authors have shown that the H reflex is potentiated by reinforcement manoeuvres, to the same extent as the tendon jerk if the reflexes are of similar size (e.g. Landau & Clare, 1964; Bussel et al. 1978; Miyahara et al. 1996; Zehr & Stein, 1999; Gregory et al. 2001). It was thought that the increased excitability of the motoneuron pool depended on a muscle spindle input from the test muscle. However, the H reflex was still potentiated when the Ia input from the test muscle was blocked by ischaemia (Bussel et al. 1978), or when local anaesthetic was used to block fusimotor axons (Clare & Landau, 1964). Recordings from spindle afferents using microneurography have yielded conflicting results: in some the Jendrassik manoeuvre and arousal did not (i) increase background discharge of muscle spindles; (ii) increase their response to stretch; (iii) change the input–output response of spindles to percussion, or (iv) change the α–γ balance (see Hagbarth & Vallbo, 1968; Hagbarth et al. 1975; Burke et al. 1980b, 1981). Contrary findings have been reported by Burg et al. (1973), Ribot et al. (1986), Ribot-Ciscar et al. (2000) and Ackerley et al. (2017). However if a γ mechanism was responsible for the reflex enhancement produced by performing the Jendrassik manoeuvre, one would expect the effects on spindle activity to be large, not small, and all studies should have had no difficulty demonstrating this same finding. Central changes in the gain of the reflex pathway occur and are sufficient to explain the reflex reinforcement (e.g. Fig. 1; Burke et al. 1981), raising questions about the relevance of any fusimotor activation. During isometric voluntary contractions there is an increase in γ drive to the contracting muscle sufficient to increase muscle spindle discharge (Vallbo, 1971, 1974), some 50 ms after the onset of the EMG activity (Vallbo, 1971). It involves an increase in static and probably also dynamic fusimotor drive (Vallbo, 1974; Kakuda & Nagaoka, 1998). Using ischaemia to block conduction in α motor axons, it could be shown that the increased spindle discharge involved γ motoneurons rather than β motoneurons (Burke et al. 1979). At the time the popular view was that coactivation of α and γ motoneurons would allow the spindle discharge to be maintained during contractions in which the muscle was allowed to shorten. Unfortunately, this is not so. In agreement with earlier studies in freely moving cats (Prochazka et al. 1976), the discharge of human muscle spindles is maintained during shortening contractions only if the movement is slow, preferably if the muscle is working against a load (Burke et al. 1978b; Vallbo & Hulliger, 1982; Al-Falahe et al. 1991). Fortunately the ensemble feedback from a number of muscles operating on a joint provides a good representation of joint movement (Jones et al. 2001b), so that the spindle contribution to kinaesthesia need not be compromised. However, it is conjectural whether the ability to modulate fusimotor drive selectively contributes to this. The movements studied in the early human work were, of necessity, limited by the risk that large free movements would dislocate the microelectrode. However, many different motor tasks have been studied with little evidence for selective or preferential activation of γ motoneurons. The protocols include maintaining an isotonic position despite loads (Burke et al. 1978a), accurate position-holding (Vallbo & Hulliger, 1982), removing some of the constraints and allowing more free movement (Gandevia & Burke, 1985), adaptation to sudden unloading during finger flexion (Al-Falahe & Vallbo, 1988), rapid voluntary movements (Al-Falahe et al. 1991), precision finger movements (Wessberg & Vallbo, 1995), and mental rehearsal of a motor task (Gandevia et al. 1997). Burke et al. (1980a) found no evidence for a selective effect on fusimotor neurons when subjects were given warning cues so that they could anticipate a signal to contract, but Papaioannou & Dimitriou (2021) report that, in a reaching paradigm, preparation for movement can involve tuning of spindle receptors. While Vallbo & Al-Falahe (1990) reported no evidence for selective fusimotor activation when learning a motor task, Dimitriou (2016) reported substantial modulation of muscle afferent discharge as a function of adaptation state when learning a visuomotor adaptation task. Similarly, Hospod et al. (2007) reported differences in the same task, dependent on whether attention needed to be focused on the task, and Ribot-Ciscar et al. (2009) suggested that ‘fusimotor drive depends on the parameter the task is focused on, so that the muscle afferent feedback is adjusted to the task requirements.’ Thus, there is evidence that the balance between the fusimotor and skeletomotor drives to a contracting muscle can be changed. In earlier studies, caloric vestibular stimulation altered the balance between fusimotor and skeletomotor drives to contracting muscle (Burke et al. 1980b). Cutaneous afferent volleys could do likewise, dependent on their site of origin: “the relationship between the skeletomotor and fusimotor drives to a muscle during a voluntary contraction is not rigidly fixed, but can be varied appropriately with the changing motor role demanded of the muscle by supraspinal drives and with the changes in sensory feed-back generated by the movement itself” (Burke et al. 1980a). With precision finger movements, Kakuda et al. (1996) concluded that ‘fusimotor activity was often stronger with precision movements compared with routine movements … higher fusimotor activity in more demanding motor tasks … effects were much smaller in humans than in cats.’ In 1995, Wessberg & Vallbo observed, that in the visual control of precision finger movements, ‘a small effect of an increased and independent gamma-activation emerged in the statistical analysis in 11% of the units.’ The evidence indicates that any ‘α/γ linkage’ is not identical in different motor tasks. It is noteworthy that the above studies have focused on the activation of fusimotor neurons, but withdrawal of fusimotor activity could also be important in some tasks. In a visuomotor adaptation task, Jones et al. (2001a) suggested that ‘the CNS reduces the sensory signals arising from muscle spindles perhaps as a means of resolving the conflict between visual and proprioceptive feedback during the task.’ In the cat, cutaneous and muscle afferent volleys can reflexly excite or inhibit dynamic and static γ motoneurons. In humans, non-noxious cutaneous inputs can alter muscle spindle discharge from tibialis anterior only when subjects are standing without support (Aniss et al. 1990). Volleys in low-threshold cutaneous afferents can alter the discharge of muscle spindles in the relaxed forearm extensors, with some evidence for a somatotopic organization (Gandevia et al. 1994). However painful stimuli are insufficient to activate spindle endings in tibialis anterior in otherwise relaxed subjects (Birznieks et al. 2008; Fazalbhoy et al. 2013) or in recumbent subjects performing an isometric contraction (Smith et al. 2019). Taken together these findings suggest that cutaneous afferents can alter the discharge of γ motoneurons selectively, but that such effects may well be task-dependent, at least in the lower limbs. It is conceivable that stimulation of cutaneous receptors during natural movements may have been responsible for some of the positive findings during movement. There are powerful mechanisms within the spinal cord for changing the strength of reflex pathways (Pierrot-Deseilligny & Burke, 2012), and it seems unlikely that controlling reflex gain is the prime role of the fusimotor system. Vallbo (1974) calculated that the gain of the reflex feedback is low, and Al-Falahe & Vallbo (1988) stated, ‘The findings lend no support for the view that the size of the stretch reflex in a behavioural task is adjusted by selective changes of the fusimotor drive.’ It is likely that the gain of spinal reflex pathways is varied centrally, rather than through a fusimotor action on muscle spindles, as in Fig. 1 (Burke et al. 1981). Figure 1B shows that performance of the Jendrassik manoeuvre did not alter the muscle afferent response to tendon percussion significantly (triangles are superimposed on circles), but that tendon jerks (filled symbols) then appeared for much weaker taps. Figure 1C shows that the gain of the reflex response was greatly enhanced, such that the same-sized afferent volley produced a much greater reflex response. The contrary view has been recently put by Horslen et al. (2013) who showed that a postural threat produced changes in the tendon jerk but not the H reflex. They concluded that ‘the muscle spindles activated in the T-reflexes must be more sensitive in the threatening conditions.’ In a further study (Horslen et al. 2018), they again attribute changes in a short-latency stretch reflex to activation of dynamic fusimotor neurons. The present author retains reservations about whether any conclusion about fusimotor drive can be made from these studies. To infer an increase in dynamic fusimotor drive from the changes in dynamic sensitivity of the short-latency stretch reflex revives an old (and long-discredited) technique for investigating fusimotor function (Burke et al. 1983). Fusimotor motoneurons can be activated preferentially, even selectively, in humans, but there is little evidence that this is a mechanism for changing the gain of stretch reflexes. The present author believes that the field has been hampered by the belief that everything functions as in the cat and that we would see this if only we could study humans behaving like cats. The optimal solution for human motor control cannot be the same as in the cat, and it is not totally unexpected that fusimotor control would differ. We have different movement repertoires: we stand plantigrade, balancing over our ankles, locomotion is bipedal, and our upper limbs are particularly well developed for fine manipulative tasks. We are much larger, our group Ia afferents conduct more slowly (cats up to 120 ms−1 vs. humans 65 ms−1; Macefield et al. 1989), and the contraction time of muscle is slower – all factors that affect whether a reflex response to a perturbation will assist or hinder movement. Assistance is more likely in the cat; hindrance may occur for some movements in humans. It may be important that the subjects for human microneurography have generally been adults, not naïve infants learning to move. The importance of the fusimotor system in human motor control may change with development. In addition, perhaps we have focused too much on the reflex effects of muscle spindle afferents, and too little on their sensory role and their importance in formulating and updating the motor programme. It is conceivable that selective changes in fusimotor drive play an important role in kinaesthesia and in providing the feedback necessary for performing and updating a movement. It is therefore pertinent that, during unobstructed aiming movements at the wrist, ‘wrist joint position was remarkably well encoded in the ensemble muscle spindle data’ and that the data were also able to encode the instantaneous trajectory of movement (Jones et al. 2001b). Readers are invited to give their views on this and the accompanying CrossTalk articles in this issue by submitting a brief (250 word) comment. Comments may be submitted up to 6 weeks after publication of the article, at which point the discussion will close and the CrossTalk authors will be invited to submit a ‘Last Word’. Please email your comment, including a title and a declaration of interest, to [email protected] Comments will be moderated and accepted comments will be published online only as ‘supporting information’ to the original debate articles once discussion has closed. David Burke is Professor Emeritus in the Department of Neurology at Royal Prince Alfred Hospital and University of Sydney, having previously held Chairs of Clinical Neurophysiology and of Neurology at the University of New South Wales. He was appointed Chairman of the Department of Neurology, Prince Henry and Prince of Wales Hospitals in 1991. He led one of the two research teams around which the Prince of Wales Medical Research Institute (now renamed ‘NeuRA’) was formed in 1991, and was Director of Clinical Research until 2002. From 2002 to 2008, he was Dean of Research for the Health Faculties at University of Sydney and from 2008 to 2013 Bushell Professor of Neurology at Royal Prince Alfred Hospital. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. None. Sole author. None.