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Clinical Commentary Coordination Training in Individuals With Spinal Cord (2006) 44, 7–10 & 2006 International Spinal Cord Society All rights reserved 1362-4393/06 $30.00 www.nature.com/sc Clinical Commentary Coordination training in individuals with incomplete spinal cord injury: consideration of motor hierarchical structures TH Kakebeeke*,1, SH Roy2 and RH Largo3 1Institute for Clinical Research, Swiss Paraplegic Centre, Nottwil, Switzerland; 2Boston University, NeuroMuscular Research Center, Boston, MA, USA; 3Department of Paediatrics, Growth and Development Centre, University Children’s Hospital, Zurich, Switzerland Study design: Clinical commentary. Objective: To discuss the method ofcoordination training to enhance motor skills in persons after spinal cord injury (SCI). Method: From the literature and clinical experience, we learn that basic motor skills like walking are refined and maintained through the millions ofrepetitions that take place as part of normal development. These coordinated patterns function effectively as a form of training to the system because ofthe presence ofneural pathways that mediate commands between higher and lower levels ofthe central nervous system (CNS). When these pathways are disrupted as a result ofa lesion, the question that arises is whether retraining can be effective. Results/Discussion: The question is directed at the common practice among rehabilitation professionals to prescribe and carry out tireless repetitions of coordinated motor activities in people with SCI lesions. We discuss this fundamental question from the perspective of understanding differences in maturation and function of higher motor centres and lower motor centres. Spinal Cord (2006) 44, 7–10. doi:10.1038/sj.sc.3101783; published online 19 July 2005 Keywords: incomplete spinal cord injury; central pattern generator; supraspinal tract; coordination training Introduction Coordinated movement demands considerable practice training ofbasic motor skills ofthe lower extremities or training.1–4 A child takes about three million steps is an effective strategy for motor relearning in those before the pattern of walking is mature at about 6 years subjects who have an incomplete spinal cord injury ofage. 1 Similarly, in sports, it is estimated that a (SCI). professional basketball player shoots as many as one million baskets before the movement is perfected.1 The importance ofcoordination training is described in Organization of the neuromotor system textbooks on motor learning3 and motor development.4 Our motor system is organized hierarchically, with the The process ofcoordinated learning, according to uppermost level mediated through the primary motor Kottke,2 involves learning to perform a movement with cortex (localized in the gyrus precentralis) and the minimal activation ofagonist muscles while inhibiting lowermost levels mediated through the spinal motor muscles that do not effectively contribute to the desired neurons. In this hierarchical structure, the uppermost activity. In the healthy human motor system, where all components are generally responsible for the initiation the prerequisites for movement are present, training of ofthe movement, whereas the lower level components coordinated activity, such as walking and running, is are responsible for the organization and execution of the effectively achieved through the many repetitions that movement (eg how to make a movement). At the occur as a normal part ofhuman motor development 4 lowermost level, all the motor commands converge on and exploration ofthe environment. In this article, we 5 the motor neuronal pool in the spine. The motor would like to focus on the question of whether the neuronal pool is a prerequisite for all muscle contrac- tions; only after a depolarization of these motor neurons *Correspondence: TH Kakebeeke, Institute for Clinical Research, can a muscle contraction take place. It is for this reason 6 Swiss Paraplegic Center, Nottwil 6207, Switzerland that Sherrington described this path from the motor Coordination training after incomplete SCI TH Kakebeeke et al 8 neuronal pool in the spine to the muscle as ‘the final treadmill training is limited.12,15,16 One reason for this common pathway’. lack of transfer is that the proprioceptive feedback of the moving feet on a stationary surface is lacking.17,18 Maturation Moreover, it was also shown that people with incom- plete paraplegia profited more from treadmill training There is evidence that the corticospinal tract in man than individuals with complete lesions.12,15,16 With this matures predominantly after birth according to a fixed in mind, it becomes very important to establish an exact program. For a review on this topic, we refer the reader diagnosis ofthe SCI immediately afterthe lesion to the article by Forssberg7 on the ontogeny ofhuman because time-consuming therapies appear to be more locomotor control. In this work it was shown that innate appropriate for the incomplete injury.12,15 Furthermore, pattern generators in the spine produce stepping at birth maintaining neuronal circuitries ‘trained’ in incomplete and that during the first years oflifeit is controlled in a SCI should make these circuitries more easily accessible piecewise fashion by higher organization centres so that for eventual regeneration or compensatory plastic infant stepping is transformed to normal plantigrade processes.17,19–21 stepping. During normal development, no additional Most lesions ofthe CNS are incomplete. 22 In animals, coordination training is needed to stimulate the out- walking ability may be regained with less than 50% of growth ofthe corticospinal tract. In a classic investiga- the spinal cord left intact.23 Recent investigations on tion on the onset ofwalking in the Hopi Indian culture incomplete SCI rats showed that even the rubrospinal by Dennis it was shown that a severe restriction of tract is able to reorganize itselfand make new sprouts movement did not influence the onset ofwalking com- and connections after a partial denervation.24 This pared to unrestricted movement in early infancy.8 This provides a basis for hope among individuals with experiment shows us that the development ofwalking incomplete SCI. behaviour is innate. When this basic motor skill has developed, the child refines this motor skill to the ever- changing environment with endless repetitions as also Discussion we learn from Kottke et al1 and Gallahue.4 Critical remarks concerning coordination training for the incomplete SCI lesion CNS lesion It is our recommendation that we cautiously bear in In the case ofa lesion to the CNS, the resulting mind the following when treating the individual with functional deficits are determined by which groups of SCI. Instead offocusing on the corticospinal tract and nerve cells are severed. The site oflesion, either in the trying to train the phylogenetically youngest part ofthe spinal cord or the brain, determines whether it may be motor system first, it may be beneficial to adopt an possible to compensate for the damage, or in the worst approach where we try to influence the motor system case, lose all capability to move voluntarily. Lesions of at the lowest level initially, namely, by influencing the the spinal cord affecting the upper motor neuron CPGs, the phylogenetically older system. From several (UMN) can clearly be distinguished from lesions of group studies,15,21,25 it was highlighted that circuitry in the lower motor neuron (LMN). Generally speaking, the human species is able to learn, especially when this after a lesion to the UMN, muscle contractions are still training is combined with loadbearing. We should possible although the highest cortical control may be consider the fact that the corticospinal tract is not the missing. In contrast, lesions on the level ofthe LMN only tract to project to the motoneurons in the spine. typically result in flaccid paresis. Furthermore, after The reticulo-, vestibulo- and rubrospinal tracts also a lesion ofthe UMN, it may be possible forthe person terminate on these motoneuron pools and these latter to relearn some movements or to compensate for them tracts may be able to compensate for a damaged in such a way that they may be able to return to corticospinal tract. To us, this approach seems more independent functioning. logical because normal motor development in the For those that suffer from severe lesions of the CNS, human proceeds from the lower level to the highest much research has been done on the central pattern level, which is the corticospinal tract. generator (CPG), the foundation level of motor control Also, we should bear in mind that extrapolations in the spine. The question arises: to what extent can we from animal experiments to humans should be done activate the CPG in case ofa spinal cord lesion? with great caution when arguing that treatments that Originally, experiments on CPGs were conducted on influence the corticospinal tract may lead to a break- spinalized cats by Grillner9 and he demonstrated that it through in SCI recovery. Anatomically and function- was possible for these animals to treadmill walk, even on ally, the corticospinal tract in cat and rat differs from a split belt operating at different speeds. Similar CPG those in higher primates and humans. In quadrupeds the studies are being conducted for treadmill walking in front legs have a different function than the arms in spinal man.10–14 Although it is possible to synchronize bipeds.26 A one-to-one transfer from experiments on and improve the EMG signals after treadmill training in mammals that use four limbs for locomotion to the humans with a complete SCI, the ability ofindividuals higher primates that ambulate bipedally is not possible. with SCI to improve their overground walking after Furthermore, one ofthe reasons why so much research Spinal Cord Coordination training after incomplete SCI TH Kakebeeke et al 9 has been done on this tract in rat and mice is that the least the same25,31 or even more2 as compared to the corticospinal tract can be anatomically located very healthy motor system.1,2 Time-consuming therapies, easily. There is a resulting overemphasis on the role of which require numerous repetitions, are bound to have this tract in quadrupedal locomotion.
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