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After nerve injury the cortical representation of the hand becomes disorganized, diminishes, or may disappear, a fact that may seriously jeopardize hand function.
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The brain is much more plastic than was previously believed, possessing a large capacity for cortical functional reorganization even at the adult stage.
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The goal of sensory reeducation is to find ways to maintain or restore cortical hand representation after nerve injury and repair.
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Following repair of major nerve trunks, there is initially a period ( phase 1 ) lasting for several months when no regenerating fibers have reached the senseless hand, followed by phase 2 representing reinnervation of the hand.
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It is our belief that sensory reeducation should start immediately after nerve repair (phase 1) to preserve the cortical hand representation.
Repair of injured nerve trunks in the upper extremity of adults usually results in incomplete recovery of sensory function in the hand. One explanation for this is that after nerve injury the cortical representation of the hand becomes disorganized, diminishes, or may disappear, a fact that may seriously jeopardize hand function. It is as if the hand “speaks a new language to the brain.” The purpose of sensory reeducation is to facilitate acquisition of the “new language” and to enhance recovery of sensory function in the hand.
It was long believed that the cortical body map was firmly established in the adult brain, but according to evolving concepts the brain is much more plastic than was previously believed, possessing a large capacity for cortical functional reorganization even at the adult stage. Rapid reorganizations occur as a result of changes in activity and sensory inflow. For example, a decrease of the cortical representation of a body part is seen as a result of anesthesia, amputation, and nerve injury. In addition, the brain possesses a cross-modal and multimodal capacity, implying that one sense can substitute for another.
A major goal is thus to find ways to maintain or restore the cortical hand representation in such situations. Not only may sensory reeducation be of importance after a nerve reconstruction, it may be equally important in situations with only a slight change in the somatosensory cortex to maintain or restore the cortical somatosensory patterns so as to facilitate the sensorimotor neural networking.
Following repair of major nerve trunks, there is initially a period ( phase 1 ) lasting for several months when no regenerating fibers have reached the senseless hand, followed by phase 2 , representing reinnervation of the hand. Each of these phases requires a specific treatment strategy, and it is our belief that sensory reeducation should start immediately after nerve repair to preserve the cortical hand representation.
The Sensational Hand—Conceptual Framework
The richness in specific tactile information from the hand, combined with the flexible processing of the brain, has made the human hand a sophisticated instrument with an enormous capacity to perceive, to execute, and to express—simultaneously—in the explorative act of touch. , A functioning sense of touch creates a base for the use of the hands, and such touch is a vital part of activity—activity that is a basic driving force in humans.
In Lettre sur les aveugles (“Letters on the Blind”), from 1749, the French philosopher Diderot discusses the role of learning in the development of normal perception, for example, that “touch gains in power owing to its use.” That is briefly what sensory reeducation and sensory relearning is about—“Use it or lose it”—and sensory reeducation is indeed a challenge in the efforts to improve a person’s function after a nerve injury.
Jean Ayres described in her sensory integration theory the dynamic relationship between behavior and neural processing of input from the senses. The brain must organize input from many sources into meaningful patterns that can be utilized for interaction with the environment and participation in daily-life activities. Such a continuous cross-modal and multimodal networking in the brain , can be used in sensory relearning. Let other senses help when touch sensibility is weak. For example, touching a fruit can systematically be associated with its taste, smell, and color, creating “a tactile meal.”
Four major modalities of somatic sensibility can be defined: touch, proprioception, pain, and temperature sense. A hierarchy of touch functions can also be identified: If detection of touch is present, the next level is discrimination of touch, basic tactile gnosis. , Localization of touch is also an aspect of discriminative touch, and identification of objects, shapes, and textures with active touching is the third level—a more refined tactile gnosis. ,
Functionality of sensation has been analyzed. An adequate feedback system for control of grip force by the integration of sensory and motor mechanisms and the proprioceptive elements has been investigated in depth, , and this knowledge is essential for sensory feedback. The superiority of sensibility in a well-coordinated hand is also emphasized, whereby sensibility and memory are discussed as key factors that control our acquired motor programs. Direct recording techniques from the cortical surface of the brain, and modern brain imaging techniques such as positron emission tomography, magnetic resonance imaging (MRI), magnetic encephalography, and transcranial magnetic stimulation have also made it possible to explore issues of tactile processing in the brain, and brain plasticity.
Napier described the hand as “an organ of touch which feels round corners and sees in the dark.” Sterling Bunnell, the father of hand surgery, described sensation as the “eyes” of the fingers, illustrated by Moberg with the classic seeing fingertips , meaning that a hand without sensibility is blind.
The expression functional sensibility is frequently used in hand surgery literature, as a basic function for what the hand can do (i.e., purposeful use of the hand). It is the subtle sensibility that gives the grip “sight,” not just to perceive but to understand the touch. Brand and Yancey also pointed out the important functional protective aspect of hand sensibility: “Pain the gift nobody wants.” Wynn-Parry and later Dellon and Curtis express this holistic view on the hand and hand sensibility, and the importance of not only motor reeducation but also sensory reeducation programs to improve poor results after nerve injuries. ,
Moberg established the term tactile gnosis in his classic articles from 1958 and 1962 as the specific aspect of functional sensibility representing the interplay between peripheral function of the nerve and the interpretation of sensory impressions in the brain. Tactile gnosis enables recognition of qualities and the character of objects without using vision. Tactile gnosis capacity is specifically addressed in sensory reeducation programs.
The hand is sometimes described as a sense organ strongly linked to the brain and to the personality. This approach has in recent years also gained importance in discussions of surgical techniques to improve poor results after nerve lesions. The emphasis in these discussions is not only on the importance of advanced surgical techniques but also on the rapidly expanding knowledge in neurobiology with several tools to influence injured neurons and to use the inherent plasticity of the neurons in further development of sensory reeducation.
Factors Influencing Outcome after a Nerve Injury and Sensory Reeducation
Nerve injuries may seriously interfere with an individual’s capacity to function adequately, and the acquired disability is often dramatic. A hand with limited sensibility is usually a hand with very limited function. There is a high probability of lost work capacity and impaired quality of life for the patient. , There is often lifelong hand function impairment, pain, dysesthesia, allodynia, and cold intolerance. There is also a substantial economic impact of nerve injuries on the patient as well as on society.
Age
Although the outcome from nerve repair is disappointing in adults, it is well-known that children usually achieve superior functional results without any formal sensory reeducation. The shorter regeneration distance in children and a better regeneration capacity in general contribute to these good outcomes. However, the superior ability of the cortex’s central adaptation to the new pattern of afferent impulses presented by misdirected axons also provides an explanation for superior recovery in children. There seems to be a critical age period for recovery of functional hand sensibility, with the best results being seen in those younger than the age of 10 years, followed by rapid decline leveling out after late adolescence. Interestingly, there is a striking analogy between this pattern and the pattern illustrating the scores of immigrants on a grammar test, plotted against the age at which they start to learn a new language. Thus, the critical period for regaining discriminative tactile capacity after nerve repair is analogous to a corresponding critical period for acquisition of a second language, indicating a strong learning component in acquisition of functional sensibility as well.
Timing of Repair, Type of Nerve, Level and Type of Injury
It is agreed that freshly transected nerves should be repaired acutely with no or minimal delay. , Early repair will substantially reduce the postoperative nerve cell death.
The type of nerve that is injured considerably influences the outcome. If a pure motor nerve is injured, the risk for mismatch between motor axons and sensory axons is eliminated, thus optimizing the accuracy in reinnervation. For pure sensory nerves such as a digital nerve, the situation is analogous.
After nerve transection there is an initial delay followed by sprouting and axonal outgrowth. A nerve outgrowth rate of 1 to 2 mm per day in humans has been suggested. In digital nerve injuries there is only a short distance separating the regenerating axons from their distal targets, while injuries at the upper arm level create different situations with longer time interval to regeneration of the hand. Nerve lesions at wrist level may require 3 to 4 months before the first signs of reinnervation in the hand occur.
A crush or compression lesion always results in better functional outcome than does total severance of a nerve trunk. The initial delay is shorter and the growth of axons proceeds at a faster rate after a crush injury than after a nerve transection. The Schwann cell basal lamina are still in continuity and can thus guide the axons back to their original peripheral targets. The correct peripheral reinnervation of crush injuries is reflected in a perfect restoration of the original cortical representational areas corresponding to the reinnervated body part. ,
Central Nervous System Factors—Cognitive Capacity
The surgeon’s ambition is to use repair techniques that bring a maximal number of nerve fibers into correct peripheral cutaneous areas. However, there are at least three strong indications that central nervous system factors associated with cortical remodeling represent a major reason for the inferior functional outcome following nerve repair. First, children up to the age of 10 to 12 years usually present excellent recovery of functional sensibility in contrast to adult patients. This critical “age window” for perfect sensory recovery presented by children corresponds well with what is known from other types of learning processes, for instance, the ability to acquire a second language. Second, cognitive functions are important explanatory factors in adults for variations in recovery of tactile discrimination. Third, the peripheral repair technique in nerve lesions has not been found to influence the functional outcome in a clinical randomized study at a 5-year follow-up. Silicone tubular repair, leaving a short distance between the nerve cuts, was compared with the outcome from routine microsurgical repair in a clinical randomized prospective study. The study included 30 patients with median or ulnar nerve injuries in the distal forearm. Postoperatively, the patients were assessed regularly over a 5-year period with neurophysiologic and clinical assessments. After 5 years there was no significant difference in outcome between the two techniques except that cold intolerance was significantly less severe with the tubular technique. The most significant improvement of perception of touch occurred during the first postoperative year, while improvement of motor function could be observed much later. In the total group there was however an ongoing improvement of functional sensibility throughout the 5 years after repair, although there was no further impairment in nerve conduction velocity or amplitude after the first 2 years. This supports the thesis that central nervous system factors associated with the cortical remodeling after a nerve repair are important, and that efforts to improve the results following nerve repair in the future must address the brain as well as the peripheral nerve.
In addition to the large number of peripheral and central factors, active and conscious use of the hand in activities of daily life, combined with high motivation by the patient, has long been reported to be of great importance for useful return of functional sensibility. Bruyns et al. found that intensive education, high compliance to hand therapy, and an isolated injury predict quicker return to work in patients with median and/or ulnar nerve injuries. A recent meta-analysis showed that age, site, injured nerve, and delayed repair significantly influence the prognosis after nerve repair. Early psychological stress has also been found to influence the outcome in a negative direction.
Cortical Remodeling—Response to Sensory Input
The human hand and the brain have developed into a sophisticated functional unit, and the hand is largely represented in the somatosensory cortex of the brain with arrangements of sharply divided territories receiving impulses from specific areas of the hand. This is reflected in the mapping of the body revealing great variation in tactile discrimination. The fingertips, lips, and the tongue, which occupy large areas, exhibit the highest resolution. However, the plasticity of the brain enables changes in the territories when the prerequisites and demands for sensory input are changed. This is a functional reorganization that is described by several authors.
According to evolving concepts over the last decades, the brain is much more plastic than was formerly believed, possessing a substantial capacity for cortical functional reorganizations also at the adult stage. , In primate experiments using techniques for direct recording from the brain cortex, , strong evidence has been presented that there is a capacity for rapid cortical reorganization in the somatosensory cortex of adult primates that may occur for several reasons, such as changed sensory experience and performance of the hand, overuse, amputation, and local anesthesia. The brain can be sculpted by experience, and this dynamic is true for the entire lifetime. The brain’s capacity for remodeling is what makes sensory reeducation and sensory relearning possible. In various neuropathies, focal hand dystonia, and during immobilization, a disorganized somatosensory cortex may be one important reason for problems with hand function.
Experience-Dependent Cortical Remodeling
Effects of Increased Sensory Input
Direct recordings from the somatosensory cortex in monkeys demonstrated experience-induced cortical remodeling secondary to increased tactile stimulation of separate fingers. , Simultaneous tactile stimulation of nearby separate receptive fields of the adult rat paw for a few hours also induces a selective enlargement of the cortical area representing the stimulated skin fields. This phenomenon has been demonstrated in experimental studies involving human subjects. Continuous co-activation of separate receptive fields in a fingertip for 2 to 3 hours results in an expansion of the fingertip cortical representation in the S1 area, a phenomenon that is linked to a significant improvement of two-point discrimination.
This is interesting from a functional point of view. Tasks requiring increased discriminatory skill relate to an expansion of the cortical projection area corresponding to the fingers involved in the task . You can see the same phenomenon in fingertips subjected to long-term massive tactile stimulation. Patients with blindness using their index fingers for reading in Braille demonstrate an expansion of the finger representation. The string hand of violin players occupies enlarged projection areas in the somatosensory as well as motor cortex of the brain. , These changes in representation have been demonstrated in other groups of professional musicians in both the somatosensory and auditory domains.
When Increased Sensory Input Becomes a Problem
Stereotypic and repetitive fine motor movements can degrade the sensory representation of the hand in the somatosensory cortex and lead to a loss of normal motor control. , This can be observed in musicians suffering from overuse syndromes such as functional dystonia (i.e., the inability to control and regulate individual finger movements). In such situations the cortical hand map is distorted and remodeled into a disorganized pattern. The physiologic basis is probably repetitive monotonous tactile stimulation and use of the hand over extended time periods. In monkeys, trained to perform monotonous repetitive hand movements involving simultaneous tactile stimulation of various parts of the hand, fusion of the normally well-separated cortical projection sites of individual fingers has been seen. The cortical “hand-glove” becomes a mitten. Reversal of the reorganization changes by use of specific training programs including very specific sensory discriminative tasks have shown good results in dystonia treatment. Some of this information is available to our readers in Chapter 135 .
Effects of Decreased Sensory Input
Diminished or complete arrest of tactile input may result in degradation of cortical representations. , Hands in persons with cerebral palsy that are contracted into severe flexion postures, devoid of sensory experiences, are associated with a diminished sensory capacity. Surgical procedures to open the hand allow for the possibility of new tactile experiences to wake up such sensibility in disguise. If the lower extremity is immobilized, its representation in the motor cortex decreases, a phenomenon that is reversible with regained mobility. Sensory reeducation may be helpful in this situation of prolonged immobilization.
Nerve Injury and Repair
After a major nerve injury there is a cortical response with an instant and long-standing reorganization of the somatosensory brain cortex. The silent area without sensory input triggers an expansion and invasion from adjacent cortical areas. This is the beginning of a dynamic interplay in the cortical neural networks, which is influenced by several biologic and psychological events during regeneration and reinnervation. These changes, which happen within minutes, are probably based on unmasking of normally occurring, but inhibited synaptic connections. There are reasons to believe that such connections are susceptible to further changes. During this postinjury period before regeneration occurs, the hand is without sensation and there is no sensory input from the areas normally innervated by the injured nerve. In the following sections this period will be named phase 1 .
The microsurgical nerve repair techniques have been refined to an optimal level; however, there is still a significant disorientation of regenerating axons at the repair site. Therefore, the skin areas of the hand will, to a large extent, not be reinnervated by their original axons. The result is additional new changes in the cortical territory where the nerve is normally represented. The original well-organized hand representation is changed to a distorted pattern ( Fig. 46-1 ). The nerve does not recapture all of its original territory. The former specific cortical representation of separate fingers disappears and changes into an overlapping pattern between the fingers. This knowledge is based primarily on primate experiments, but analogous findings have been made also in humans on the basis of functional MRI techniques. The specific cortical territories representing each finger in primate experiments have shown a completely changed pattern. The hand speaks a new distorted language to the brain, requiring a relearning process. This is referred to as phase 2 , representing reinnervation of the hand. After a nerve injury at the wrist level, phase 2 usually begins 3 to 4 months after nerve repair. The timing for onset of sensory reeducation may be of critical importance. Each of the two phases following a nerve repair requires a specific treatment strategy, and we suggest that sensory reeducation should start immediately after nerve repair to preserve the cortical hand representation.
In summary, there are good reasons to look for factors in the central nervous system, in addition to the cellular and biochemical events, that are associated with degeneration and regeneration in the peripheral nervous system to explain the incomplete sensory recovery after nerve repair. A nerve injury in the upper extremity is followed by profound functional reorganization changes in the brain cortex, mainly due to misdirection of regenerating axons. These central events, which are an expression of the brain’s capacity for rapid plasticity, play a predominant role in the sensory reeducation programs of today. This is a challenging and important area for multidisciplinary clinical development and research in the field of rehabilitation following nerve injuries.
Sensory Reeducation—Principles and Planning
The practice of sensory reeducation has long existed in rehabilitation settings along with motor reeducation but was not recognized as such until Wynn-Parry and Dellon designed the first formal programs. The functional improvement seen after training may be based on normalization of the distorted hand map, or it may be due to adaptations in higher brain centers with a capacity to decipher the distorted hand map. Further study is needed to determine which explanation is correct.
Learning is a key word in the rehabilitation process after all injuries. New sensory and motor codes are presented to the brain with which the brain must cope for purposeful sensorimotor interaction and functional use. A relearning process is required to adapt to the new and distorted afferent sensory input when familiar objects are touched. The mind does not understand the new “sensory code” associated with specific textures and shapes. To facilitate and enhance this process, specific programs for sensory reeducation are routinely used for regaining tactile gnosis. According to these strategies, the brain is reprogrammed on the basis of a relearning process. Sensory reeducation is based on vision guiding touch and on higher cortical functions such as attention and memory during several daily short practice sessions occurring over several weeks or months. , With active use of the hand, the patient learns to code the integrated passive and active afferent stimuli with slower and fewer conducting nerve fibers than normal. ,
The sensory reeducation training is integrated in the overall rehabilitation program and individualized based on the patient’s level of sensory function. As mentioned previously, following repair of major nerve trunks there is initially a period ( phase 1 ) lasting for several months when no regenerating fibers have reached the senseless hand, followed by phase 2 representing reinnervation of the hand. Each of these phases requires a specific treatment strategy.
In phase 1 there is no protective sensibility, and it is important to carefully watch the hand during use to prevent skin injuries. The lack of protective sensation is an important message to communicate to the patient in this early phase. In phase 2 the axons have reached the hand. Hypersensitivity to normal touch is common during this period. If so, desensitization exercises should precede the training sessions. Hyperesthesia and allodynia and its treatment are described elsewhere in Chapter 113 , Chapter 114 , Chapter 115 , Chapter 116 .
Specific, simple, and repetitive sensory relearning exercises of increasing complexity and difficulty should be performed at home by the patient on a daily basis in frequent brief training sessions. Weekly training sessions with the therapist may be scheduled to provide guidance and feedback. Training in a quiet location for high attention is recommended, and active and conscious use of the hand in daily activities combined with high motivation by the patient are important factors. The rehabilitation after a nerve repair is a long process that can take several years, so it takes a lot of patience. The complexity after a nerve injury with interacting phenomena that depend on so many factors is not easy for the patient to understand. Therefore, the information and education of the patient about the injury and the sensory reeducation concept are crucial. If the patient does not understand the training concept, it is very difficult for him or her to be motivated to follow through with the retraining. A written home program should always be given to each patient. The patient should also be encouraged to use the affected hand very consciously in daily activities.
Timing—Onset of Sensory Reeducation
In the sensory reeducation program proposed in this chapter, the training technique is the classical one according to Wynn-Parry and Dellon, , but focus is on the timing of initiation of the training program not only in phase 2 but also in phase 1. The strategy is to activate the cortical area representing the damaged nerve, thereby diminishing the cortical reorganization and maintaining the cortical hand map. Borsook et al. demonstrated that following amputation of the hand, touch of the face, being close to the hand in the cortical body map, gives rise to phantom sensations as soon as 24 hours after injury. Weiss et al. demonstrated plasticity after finger amputation within 10 days after amputation. An analogous phenomenon can also be seen after local anesthetic blocks that temporarily can induce shifts in neuronal receptive fields with cortical reorganization.
The traditional procedure calls for the introduction of sensory reeducation once touch can be perceived in the involved area. , However, at this point the reorganizing brain presents a random pattern, which may not be possible to reverse. Cheng et al. presented a prospective randomized study on early tactile stimulation after digital nerve repair (3 weeks after surgery) that showed excellent results and significantly better discriminative sensibility in the study group. If the “vacant” cortical area of a denervated hand could be provided relevant information from the hand using visual clues early after repair, it might help to minimize the synaptic reorganization. This may well make the brain better prepared for the relearning program once the nerve has regenerated and reinnervated the peripheral targets.
The design and protocols of the sensory reeducational programs have not changed over the last decades. This is surprising, considering the enormous advances in neuroscience and brain imaging techniques that have increased our understanding of mechanisms underpinning brain plasticity. We therefore have presented new strategies for sensory reeducation that utilize the capacity for cross-modal and multimodal capacity of the adult brain as well as the remodeling capacity of the brain.
Sensory Reeducation in Phase 1—Sensory Preparation
In phase 1 we focus on maintaining the cortical hand representation by using the brain’s capacity for sensory imagery as well as cortical visuo-tactile interaction. Phase 1 lasts until there is measurable sensibility present in the hand that can be assessed with Semmes–Weinstein monofilaments. To be able to start sensory reeducation at this critical early stage without any existing sensibility in the hand, we use the holistic organization of the brain with an extensive capacity for cross- and multimodality. The sensory relearning in this early phase, in combination with mobility training of the hand, is aimed at activating and maintaining the hand map in the brain to make the sensory relearning easier once the axons have regrown. This gives the brain an illusion of sensibility in the hand.
The use of vision to guide the retraining of sensation is the basis for classic sensory reeducation, but there is a continuous interplay among all senses. Multisensory neurons that receive more than one type of sensory input may be used to extract information from one sensory modality and use it in another by using polymodal association areas.
The multimodal capacity of the brain and brain’s capacity for adaptation with deprivation of sense can be illustrated in individuals with blindness. When such a person reads Braille or carries out other tactile discrimination tasks, the primary visual cortex is activated together with the somatosensory cortex.
Sensory Imagery
Similarities exist in the cortical functions between perception and imagery. Auditory cortical areas are recruited in the absence of sound during imagining music, the visual cortex is active during visual imagery, and imagination of odors is associated with increased activation in olfactory regions in the brain. Just imagining a movement activates the premotor cortex. The pattern of somatosensory activation during motor imagery is very similar to the pattern observed during a real movement execution. Few observations of sensory imagery with involvement of primary sensory cortical areas have been reported. Just thinking about stroking the dorsum of the hand activates the sensory cortex. It is recommended that the patient can try to imagine touch in the hand during phase 1.
Observation of Touch, Reading or Listening to “Sensory” Words, Observing “Sensory Pictures,” Mirror Training
Activation of motor neurons that may also serve as mirror neurons in the premotor cortex by the observation of hand activity is a well-known phenomenon, which is believed to play a fundamental role in both action and imitation. Mirror neuron areas are also involved in understanding the intention of actions. Reading or listening to action words related to hand movements activates hand representational areas in the motor cortex, and hypothetically reading or listening to “sensory” words or watching “sensory” pictures would relate to activity in the somatosensory cortex. Other ways to activate the somatosensory cortex include observing a body part being touched. Keysers showed this during observation of touching the legs, and we have demonstrated a visuo-tactile cortical interaction during mere observation of tactile stimulation of the hand. It is suggested that the somatosensory cortical areas, SI and SII cortex, are related to the mirror neuron system. The patient’s observation of his or her hand being touched is one component of early sensory training the first day after surgery, which might activate the cortical hand area due to visuo-tactile interaction ( Fig. 46-2 ).
