By Rebecca H. Martin, OTR/L
There is a paradigm shift happening in rehabilitation, a shift that has been championed for more than a decade at Kennedy Krieger Institute’s International Center for Spinal Cord Injury in Baltimore. Rehabilitation interventions targeting restoration of function lost to injury are being prioritized, for the first time, over interventions aimed at teaching patients to compensate for lost function after a spinal cord injury or stroke.
This is happening for a number of reasons. First, scientific evidence continues to demonstrate that the nervous system is capable of change and repair, but that process is activity-dependent. Second, rehabilitation strategies specifically aimed at restoration have become more prevalent and available outside of specialty centers like ours. Finally, patients themselves are pushing aside the “old” limits and expectations and asking more from their therapists, refusing to live statically from a wheelchair.
This shift is further bolstered by research suggesting that when working only to strengthen and improve function in an area of the body less affected by injury, the disuse and dysfunction of the impaired area actually increases.1 Essentially, compensation training decreases the potential for restoration of function, reinforcing the “use it or lose it” mantra.
The value of restorative interventions goes beyond generalizable improvements in function and independence. Patients also experience greater skill retention and secondary complications; and comorbidities, such as pressure sores and respiratory illness, are reduced. The benefits are clear and achievable in many rehabilitation environments.
The Role of Activity
Historically, the word “activity” was used interchangeably with “exercise,” but that, too, has shifted as clinicians learn about the critical role of activity in recovery. Activity-based restorative therapy utilizes patterned activity intended to restore motor and sensory function, using near normal kinematics and conditions with high-volume repetition.
The science of neural plasticity, the capacity of the nervous system to undergo changes in function and structure in response to use and motor learning, offers further understanding into the restorative process. When synaptic efficacy is altered through increased or decreased excitability, latent connections are unmasked and new connections are formed through sprouting and synaptogenesis.
Activity helps to optimize the nervous system environment for recovery. It encourages the proliferation of endogenous glial cell progenitors that, as they become oligodendrocytes, remyelinate demyelinated axons. Further, activity may help to decrease the death of oligodendrocytes from chemical reactions of damaged cells. Therefore, treatments that elicit motor activity, especially those that activate afferents as well as efferents, are likely to promote repair of damaged myelin.
Cells to support and restore myelin are dormant in a damaged nervous system. Activity mobilizes endogenous cells (schwann cells and oligodendrocyte progenitor cells) to take advantage of spared axons, improving their efficiency. Without the need to bypass the zone of damage, direct regrowth, or accurately synapse, remyelination is a much more reasonable goal to improve the central nervous system.
While the evidence overwhelmingly supports high-volume activity-based interventions, the current environment of care does not always allow for them. Third-party payors put emphasis on function and lengths of stay that often are not long enough to allow for changes in the nervous system. By incorporating priming activities, clinicians drive up the activity essential to optimize the nervous system while still making space and time for patients to complete necessary functional skills training.
Understanding the Role of Priming
Priming activities ready the nervous system for change, enhancing the effects of rehabilitation. By targeting underlying neural mechanisms, priming induces neural plasticity thereby reducing impairment and improving function. By adding priming activities to traditional rehabilitation approaches, clinicians can help to restore function lost to paralysis, not just train patients to work around it. The stimulus provided in priming activities prompts behavior change; it has been long studied in psychology and over the past half-decade has been applied in rehabilitation research studying motor priming as a means to facilitate motor learning.
Pharmacology-based priming is the oldest priming tool used, yet research primarily remains in the animal model. There are five groups of pharmacological agents, each of which targets a specific neurotransmitter and disease group:
- Amphetamine increases neuroepinephrines to accelerate recovery of function in traumatic brain injury and stroke.
- Dopaminergic agents increase synaptic plasticity and motor memory in Parkinson’s disease.
- Norepinephrines enhance plasticity and mediate learning and memory.
- Cholinergic agents have been widely studied in multiple sclerosis.
- Serotonin re-uptake inhibitors improve function in patients with stroke, multiple sclerosis, and epilepsy.
Motor imagery and action observation priming describes a motor task that is internally rehearsed within working memory without any overt motor output. It is understood that this increases regional cerebral blood flow and influences corticospinal excitability. Priming activities in this category are commonly referred to as mental practice and include: action observation, mirror therapy, computer-directed imagery, audio-tape generated imagery, and therapist-directed imagery. Research shows that mental practice in combination with physical practice was more effective in improving upper extremity function in those post-stroke than physical practice alone.2 Clinicians should be mindful that mental practice priming activities are task specific and skill enhancement does not generalize well.
Movement-based priming is any repetitive or continuous movement in conjunction with other therapeutic activities. It typically includes bilateral movements, mirror symmetric movements, balance components, and aerobic exercise. The increased activity increases expression of brain-derived neurotrophic factor (BDNF) and increases corticomotor excitability. BDNF supports the survival of existing neurons and encourages growth and differentiation of new neurons and synapses. Movement-based priming activities also improve aerobic fitness, learning, and enhance cognitive flexibility.
Patients with subacute and chronic stroke, who participated in motor-based priming, performed better on the Action Research Arm Test (ARAT), as compared to patients in traditional rehabilitation.3-5 Promising results are also being seen in patients with Parkinson’s disease.6
Successful clinical application consists of high intensity, bilateral, often symmetrical activities, including rhythmic arm-swing, upper extremity ergometry, pedaling, and use of a wrist rocker board.
Stimulation-based priming consists of four categories:
- Transcranial magnetic stimulation (rTMS) involves rapidly changing magnetic fields to induce current in the neural tissue which will excite or inhibit activity of the cortical neurons. Depending on the rate applied, it changes the level of excitability of the corticospinal system.7
- Transcranial direct current stimulation (tDCS) provides direct stimulation through an electrode on the scalp over the targeted cortical region. Unlike rTMS, tDCS changes the effectiveness of synaptic transmission within the cortex.8
- Paired associative stimulation (PAS) pairs pulses from cortical stimulation in rTMS with peripheral nerve stimulation (PNS). It combines cortical motor circuits with somatosensory input (sensory input).
- Peripheral nerve stimulation (PNS), or electrical stimulation, has long been used in rehabilitation to stimulate the motor nerves and activate muscle responses. Surface electrodes are placed over a muscle to stimulate an intact peripheral nerve, generating a muscle contraction. PNS is most commonly used in clinical applications. Electrical stimulation has been shown to reverse muscle atrophy and improve muscle composition and profusion.8
Sensory priming encompasses both sensory stimulation and sensory deprivation, and includes temporary deafferentation, vibration, and electrical stimulation. By promoting changes in the somatosensory cortex, it influences the motor cortex to improve sensory and motor function, normalize potentials, and reduce or promote cortical inhibition.
Sensory priming includes:
- Temporary deafferentation is often used in stroke rehabilitation, typically with mechanical (eg, tourniquet) or pharmacological mechanisms (eg, anesthetic cream) prior to motor training of the hand. Reduced sensory input induces increased somatosensory cortical excitation. The somatosensory cortex has to work harder to make up for what it has lost. When sensory input is then normalized, the cortical excitability is maintained, resulting in enhanced performance. Clinicians should take note that reducing somatosensory input may pose a safety risk.
- Vibration can be applied to the agonist or the antagonist muscle(s) to improve function (excitatory) and to decrease spasticity (inhibitory). Studies typically utilize 1- to 3-minute bouts, repeated three to four times with 1- to 2-minute rest breaks in-between.
- Electrical stimulation involves excitation of a peripheral sensory or motor nerve to drive a desired sensory or motor response. Sensory stimulation may assist in increasing local cortical representation to improve control of a particular motor response, while motor stimulation drives movement and associated afferent input to the CNS. It is a great alternative for those without the physical and cognitive endurance to participate in extensive training.10
Dose, Intensity, and Effectiveness
Not surprisingly, the evidence for priming activities suggests that more is better. But, there is hope for the busy therapist, with evidence to suggest that some is better than none.
A study published by our team looked at the influence of repetitive NMES-assisted grasp and release on the paretic tetraplegic hand.9 Three patients with cervical SCI underwent eight 30-minute sessions over 2 weeks. During training, patients provided triggered NMES to assist them with grasping and then releasing balls into a container. Patients demonstrated statistically significant improvements in grasp strength, speed, and prehension quality, suggesting that even a short-term intervention may produce meaningful results. Improvements were maintained 24 hours after training, also suggesting that the changes in the nervous system induced by priming may be durable.
Gomes-Osman and Field-Fote11 demonstrated that rTMS and repetitive task practice improved skill performance by 200%, as compared to repetitive task practice alone in only three 1-hour sessions. More importantly, the results were duplicated with peripheral nerve stimulation and repetitive task practice, which is easily implemented in clinical settings.
Additional studies report improvements in performance with more consistent application, five 1-hour sessions a week for 12 weeks, and multiple priming inputs, motor-based with stimulation-based.12
Structuring a session around restorative goals may be challenging at first. Clinicians have to balance providing the necessary input and activity to the nervous system with skills training. The payoff, however, is worth it. Restoration of grasp function, for example, allows patients to brush their teeth, feed themselves, and complete work tasks. By returning patients to multiple activities, clinicians ensure greater skill retention, generalizable improvements in independence, and reduced secondary complications, associated with overuse syndromes and abhorrent kinematics.
It is helpful to think about structuring sessions into three phases—priming and preparation, massed practice, and task-specific practice—plus a home-based training.
During priming and preparation, therapists use activities and modalities targeted at increasing neural excitability and preparing the physical system. The nervous system has to be engaged during priming activities, through voluntary movement, stimulated movement, or mental imagery. Clinicians may find it helpful to build in mini-priming breaks throughout a session to provide a boost of input to the system.
For example, if the goal of the priming intervention is pain management, transcutaneous electrical nerve stimulation (TENS) is a better choice than heat. A patient passively absorbs heat, while TENS will help to activate sensory nerves and modulate the pain response. If the goal is tone management, vibration, where the nervous system is bombarded by afferent input, will be more beneficial than stretching alone. And if increasing the patient’s available range of motion is the goal, therapists can turn to functional electrical stimulation as active-assistive range of motion rather than passive range of motion only.
Massed practice describes an intervention in which repetitive practice is the primary therapeutic factor used to promote cortical reorganization, and improved strength and range of motion. Massed practice includes task-specific and non-task-specific activities that are repeated multiple times for multiple hours/days. These therapist-directed activities are aimed at improving skill components.
In 2009, Lang et al13 collected data from 312 therapy sessions in acute post-stroke rehabilitation. In a “60-minute” session, patients were really only getting 36 minutes of therapy, and the amount of activity patients were engaged in was really minimal—less than one repetition per minute. It is simply not enough to drive cortical reorganization and neural change.
In 2014, her group conducted a study to assess the feasibility of massed practice interventions in that same inpatient rehabilitation setting.14 Study subjects were provided 4 days a week of individually tailored, high volume, upper extremity skills training, aiming for 300 repetitions or more in a 60-minute session. Study subjects also participated in 2 days a week of standard skills training. Patients in the study were, on average, completing 289 repetitions and engaged for 47 minutes of their 60-minute session. Perhaps more importantly, their upper extremity capacity, as measured by the ARAT, was significantly better and their skill performance, as measured by the FIM, was not significantly different from patients who received standard care. Not only was the massed practice feasible and beneficial, it did not inhibit skill acquisition.
And it is not difficult to do. Clinicians may consider breaking down functional skills into smaller pieces and using facilitation techniques to encourage normal kinematics. For example, when practicing rolling with a patient, rather than teaching them to swing their arms or reach for a bed rail, practice half rolls from a position of flexion, use Proprioceptive Neuromuscular Facilitation (PNF) techniques to encourage mass flexion, and add some electrical stimulation to their abs. All priming techniques, aimed at achieving a functional task.
During task-specific practice, incorporate priming strategies in context specific motor tasks such as standing, to increase afferent input, at the sink to brush teeth or high repetitions of elbow flexion followed by self-feeding. Training should be for a specific functional task, rather than aimed at the impairment. Weight bearing and functional electrical stimulation help facilitate afferent input, but a patient’s own efferent effort is more important. Weight-bearing enhances the outcome, but the voluntary effort of the patient is the most important. The nervous system needs his/her efferent input, while the therapist provides afferent input.
A home-based program should be an extension of an in-clinic session. Patients should be provided with specific exercises aimed at achieving collaboratively defined goals.
Dr Williams is a 64-year-old, right-handed male diagnosed with an incomplete central spinal cord injury (C3 AIS D) secondary to a fall from a bicycle. His primary complaints are shoulder pain and limited fine motor function, which prevents him from his favorite hobby: woodworking. Prior to his injury, Dr Williams was a foot surgeon.
If we use these priming principles to work toward his restorative goals, a session might look something like this:
Priming and preparation: Electrical stimulation to wrist extensors with 1- to 2-pound weight.
The goal of this part of the session is to fire up the nervous system through peripheral nerve stimulation. Using weight assists with muscle hypertrophy and local perfusion, the patient was readied for the skilled part of the session. Vibration would be a nice alternative to provide activity into the system through dorsal root afferents.
Massed practice: A rotating series of simulated repeated woodworking tasks with clinic supplies: 5 minutes of sanding, using a screw driver for 15 screws, assembly of 15 nuts and bolts. The series would be rotated for 30 minutes. Somatosensory stimulation could be applied to the palmar and dorsal surfaces of each hand as the patient begins to fatigue.
The series of activities target specific components of meaningful tasks. This allows the clinician to provide directed feedback and physical assistance as needed to remediate any component-level dysfunction. Adding the somatosensory stimulation helps to increase cortical excitability, making it possible for the patient to continue the activity, beyond initial fatigue. Therapists might also use virtual reality or gaming technology to encourage high-volume repetition of remedial skills.
Task-specific practice: Therapist-directed assembly task, using parts and tools the patient brought from home.
Putting the task back together in a context-rich environment brings meaning and generalizability to the previous practice. The patient can see how he might really work on this task at home, which he will be expected to do. At the next session, the patient should report the parts of the task that remain difficult for him. The clinician should rank these in complexity and use the lower level skills as the basis for the massed practice in the next session. RM
Rebecca H. Martin, OTR/L, is the manager of clinical education and training at the International Center for Spinal Cord Injury at Kennedy Krieger Institute. She is a practicing occupational therapist specializing in activity-based rehabilitation and the restoration of function through applications of electrical stimulation. www.kennedykrieger.org. For more information, contact [email protected].
- Allred RP, Maldonado MA, Hsu JE, Jones TA. Training the “less-affected” forelimb after unilateral cortical infarcts interferes with functional recovery of the impaired forelimb in rats. Restor Neurol Neurosci. 2005;23(5-6):297-302.
- Barclay-Goddard RE, Stevenson TJ, Poluha W, Thalman L. Mental practice for treating upper extremity deficits in individuals with hemiparesis after stroke. Cochrane Database Syst Rev. 2011 May 11;(5):CD005950.
- Stinear CM, Barber PA, Coxon JP, Fleming MK, Byblow WD. Priming the motor system enhances the effects of upper limb therapy in chronic stroke. Brain. 2008 May;131(Pt 5):1381-1390.
- Stoykov ME, Corcos, DM. Bilateral priming followed by task specific training can improve moderate to severe post-stroke upper extremity hemiparesis. Stroke. 2013;44:AWMP89.
- StoykovME, Madhaven S. Motor priming in neurorehabilitation. J Neurol Phys Ther. 2015 Jan;39(1):33-42.
- Hirsch MA, Farley BG. Exercise and neuroplasticity in persons living with Parkinson’s disease. Eur J Phys Rehabil Med. 2009 Jun;45(2):215-29.
- Dafotakis M, Grefkes C, Wang L, Fink GR, Nowak DA. The effects of 1 Hz rTMS over the hand area of M1 on movement kinematics of the ipsilateral hand. J Neural Transm (Vienna). 2008 Sep;115(9):1269-74.
- Madhavan, S, Shah, B. Enhancing motor skill learning with transcranial direct current stimulation – a concise review with applications to stroke. Front Psychiatry. 2012;3:66.
- Martin R, Sadowsky C, Obst K, Bamford B, McDonald J. Functional electrical stimulation in SCI: from theory to practice. Topics in Spinal Cord Injury Rehabilitation. 2012;18(1):28-33.
- Martin R, Silvestri J. Current trends in the management of the upper limb in spinal cord injury. Current Physical Medicine and Rehabilitation Reports. 2013;1(3):178-186.
- Gomes-Osman J, Field-Fote EC. Cortical vs. afferent stimulation as an adjunct to functional task practice training: a randomized, comparative pilot study in people with cervical spinal cord injury. Clin Rehabil. 2015 Aug;29(8):771-782.
- Field-Fote EC, Roach KE. Influence of a locomotor training approach on walking speed and distance in people with chronic spinal cord injury: a randomized clinical trial. Phys Ther. 2011 Jan;91(1):48-60.
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- Waddell KJ, Birkenmeier RL, Moore JL, Hornby TG, Lang CE. Feasibility of high-repetition, task-specific training for individuals with upper-extremity paresis. Am J Occup Therapy. 2014;68:444-453.