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Plasticity of Motor Systems

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It has been reported that 55% of all spinal cord injured persons are classified as having complete injuries. Magnetic resonance imaging (MRI) and histopathology indicates that approximately 65% of the traumatic injuries initially classified as ‘neurologically complete’ (absence of sensory and motor function in lowest sacral segment) show some tissue and axonal sparing across the lesion (Bunge et al., 1997). It is now accepted that the CNS is capable of substantial reorganization, especially in incomplete SCI because cortical, subcortical and much of the local spinal cord circuitry remains largely intact and still partially interconnected by unlesioned fibres (Raineteau & Schwab 2001). Information may still pass through the level of the lesion on spared fiber tracts, but the information may be fragmented or distorted (Beekhuizen & Field-Fote 2005). Functional recovery can occur for several years after injury in incomplete SCI, with the degree of recovery dependent upon the reorganization of circuits that have been spared by the lesion (Green et al., 1999). Cortical reorganization occurs after SCI with evidence that the sensorimotor cortex may play a role in the recovery of function in individuals with SCI (Green et al., 1999). Results of neuroimaging and neurophysiological techniques (functional magnetic resonance imaging (fMRI), transcranial magnetic stimulation (TMS) and positron emission tomography (PET) demonstrate that changes occur in the cortex following damage to the spinal cord with expansion of cortical areas corresponding to muscles spared after SCI into the cortical areas previously associated with control of muscle reinnervated at spinal cord levels below the level of the lesion (Bruehlmeier et al., 1998; Cohen et al., 1991; Levy et al., 1990; Raineteau & Schwab 2001).

In SCI, reorganization might occur at two levels; in pre-existing circuits by modifications of synaptic strength (synaptic plasticity) or by new circuits through sprouting or anatomical reorganization, including growth of axonal branches and dendrites (anatomical plasticity) (Raineteau & Schwab 2001). Laboratory work is currently explaining and researching cortical reorganization, cortical plasticity, sub-cortical plasticity, plasticity at the red nucleus, plasticity and spontaneous adaptation of the central pattern generators and plasticity of unlesioned descending pathways. The strengthening and weakening of synapses, axonal and dendritic sprouting can occur at different levels of motor system in response to spinal cord lesions, in the cortex, the brainstem, and the spinal descending pathways and in the intraspinal circuits. All interact with each other; therefore, it is difficult to interpret functional recovery processes. A SCI interrupts distinct descending fibre populations; the overall complexity of an incomplete SCI resides first in the organization of descending spinal tracts. Most of the descending systems terminate on spinal interneurons, but some direct excitatory or inhibitory connections to motor neurons also exist. Different tracts are involved in specific functions. For example, lesions of the cortical and rubrospinal systems lead to more severe and longer lasting deficits for movement of the distal extremities and lesions of the reticulo and vestibulospinal systems affect movements of proximal and axial muscles. Functional outcomes of given spinal cord lesions therefore depend on the type of fibres that are interrupted (Raineteau & Schwab 2001).

Functional reorganization is based on two mechanisms; synaptic plasticity in pre-existing circuits and sprouting and anatomical reorganization that leads to the formation of new circuits. The study of animal models provides further understanding of rehabilitation treatments and development of new therapeutic approaches for people with SCI (Raineteau & Schwab 2001).

Traditional approaches to improving arm and hand function in persons with tetraplegia generally use compensatory strategies to have the muscles that are intact substitute for the lost function of the weakened or paralyzed muscles and management of musculoskeletal complications as described in the Guidelines for Clinical Practice for the Consortium for Spinal Cord Medicine Clinical Practice Guidelines supported by the PVA 2005 (Backus 2010).

Based on the neuroplasticity research, there is a belief that there are similarities between incomplete tetraplegia after SCI and hemiplegia after stroke as incomplete tetraplegia often have altered and inappropriate sensory input and motor output and not simply the loss of sensory or motor function (Backus 2010). Persons with hemiplegia who have altered (but not absent) sensory perception and paresis (but not complete paralysis) demonstrate disordered motor control in the ULs which include the ability to balance agonist and antagonist muscles (Chae et al., 2002; Levin et al., 2000), strength imbalances (Lum et al., 2002), disruptions in initiation and cessation of movement (Chae et al., 2002) and inappropriate muscle activation (Kamper et al., 2001). Persons with tetraplegia, much like hemiplegia experience the inability to effectively activate and deactivate (relax) muscles at appropriate time and extent. The difficulty is seen in being able to control the strength or force output during movement and the altered timing and control of movement at a joint or across multiple joints. Based on this, it is thought that ISCI closely resembles hemiplegia (Backus 2010).

There are several principles underlying the facilitation of neural plasticity and functional recovery such as intense activity, repeated practice, attention and somatosensory augmentation concurrent with movement practice. The interventions usually combine intense, repetitive and often rhythmical input to CNS below the level of injury. These principles are the basis for constraint induced movement therapy approach and activity based intervention (ABint) (i.e., treadmill training, FES approach, constraint-induced therapy). The goal of ABint is to facilitate long term changes in spinal and cortical circuits and improve overall function after neural injury or disease. Until the past decade, studies researching the use and effectiveness of ABint for improving function and potentially neural activity in arm and hand in persons with tetraplegia have been scarce in the upper limb literature (Backus 2010). The research studying the use of massed practice (MP) and/or somatosensory peripheral nerve stimulation (SS) have demonstrated potential for both neural and functional improvements in persons with tetraplegia (Beekhuizen & Field-Fote 2005; Beekhuizen & Field-Fote 2008; Hoffman & Field-Fote 2007).

Seven studies were found that tested the use of MP, SS, transcranial direct current stimulation (tDCS), transcutaneous electrical nerve stimulation (TENS), vibration therapy, and repetitive transcranial magnetic stimulation (rTMS) in changing the cortex.

Table 6: Plasticity of Motor Systems

Discussion

Beekhuisen and Field-Fote (2005) suggested that MP or constraint-induced therapy promotes cortical reorganization that may be an effective rehabilitative tool for improving strength and function in individuals with cervical SCI. Improvement may be further enhanced by the addition of somatosensory stimulation. Beekhuisen and Field-Fote (2008) showed that the use of MP with somatosensory peripheral nerve stimulation (SS) and the use of SS only showed significant improvements in upper extremity function and pinch strength when compared to the results demonstrated by the control group. The study also showed that use of MP and SS together had a significant change in sensory scores and the MP with SS and MP groups only showed greater change in threshold measures of cortical excitability when compared to the control group results. These findings were supported in a more recent study (Nasser et al., 2014), however, Nasser et al (2014) also found that the combination of MP and SS resulted in a greater improvement than MP alone (Nasser et al., 2014). The mechanism of how SS and FES improves hand functioning has also been studied (Hoffman & Field-Fote, 2013). In unimanual and bimanual SS and FES conditions only a significant effect of time was found, regardless of intervention, with each condition resulting in improvements of hand functioning.

Multisensory visuo-tactile bodily stimulation has also been tested and illusory ownership over the hand was found to be more likely to occur in the presence of upper spinal levels (Scandola et al, 2014). Belci et al. (2004) observed clinical changes consistent with the concept that reduced corticospinal inhibition can facilitate functional recovery. Recovery involved increased AIS sensory and motor scores, improved response to cutaneous electrical stimulation over the thenar muscles and possibly improved hand/finger function. This preliminary study demonstrated rTMS treatment in patients with chronic stable incomplete SCI can produce reductions in corticospinal inhibition detectable using electrophysiological techniques. A more recent RCT found that rTMS resulted in improvements in hand functioning but not grasp strength or motor threshold (Gomes-Osman & Field-Fote, 2014).

One study tested the use of transcutaneous electrical nerve stimulation (TENS), transcranial direct current stimulation (tDCS), and vibration therapy (Gomes-Osman & Field-Fote, 2015). Authors concluded that TENS, tDCS, and vibration therapy resulted in significant improvements in hand functioning when combined with functional task practice.

For restorative strategies to be feasible for use in everyday clinical practice it is important that the interventions be available in the clinic and at home (Beekhuizen & Field-Fote 2005).

Conclusion

There is level 1a evidence (from three randomized controlled trials; Bekkhuizen & Field-Fote 2005, 2008; Hoffman & Field-Fote 2013) that showed that massed practice (repetitive activity) and somatosensory stimulation (median nerve stimulation) demonstrated significant improvement in upper extremity function, grip and pinch strength required for functional activity use.

There is level 1b evidence (from one randomized control trial; Gomes-Osman & Field-Fote, 2014) that showed that rTMs treatment in individuals with chronic stable SCI may produce reductions in corticospinal inhibition that resulted in clinical and functional changes for several weeks after treatment.

There is level 2 evidence (from two randomized controlled trials; Gomes-Osman & Field-Fote, 2015; Hoffman and Field-fote, 2010) that showed that tDCS, TENS, vibration therapy and repetitive massed practice resulted in significant improvements in upper extremity function and pinch strength.

There is level 4 evidence (from one post-test study; Scandola et al., 2014) that showed that the induction of the rubber hand illusion through synchronous multisensory visuo-tactile bodily stimulation resulted in ownership of the hand.

There is level 4 evidence (from one pre-post study; Belci et al., 2004) that showed therapeutic TMS can lower intracortical inhibition, which is linked to better clinical motor scores. 

There is level 4 evidence (from one pre-post study; Nasser et al., 2014) that showed massed practice and somatosensory stimulation significantly improved motor function and pinch grip strength compared to traditional rehabilitation programs over time.

  • Afferent inputs in the form of sensory stimulation associated with repetitive movement and peripheral nerve stimulation may induce beneficial cortical neuroplasticity required for improvement in upper extremity function.

    Repetitive activity combined with somatosensory stimulation can significantly increase the functionality of upper extremities, potentially improving the over all quality of life for patients.

    Restorative therapy interventions need to be associated with meaningful change in functional motor performance and incorporate technology that is
    available in the clinic and at home.