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16

Loss of somatic sensation

Leeanne Carey

Evidence of behavioral recovery of somatic sensations such as Kandel, Schwartz and Jessell (Gardner and following peripheral and central nervous system Martin, 2000). Further, neuroimaging studies are lesions challenges therapists to not only understand complementing and extending information gained the nature and extent of the change, but the condi- from animal and lesion studies in humans (Schnitzler tions under which the recovery can be maximized and et al., 2000). the mechanisms underlying. This challenge requires Two features of the structure and function of the input from basic sciences and rehabilitation fields. system have particular implication for understanding Integration of these fields will provide direction for the nature of impairment and neurorehabilitation. the development and testing of scientific-based inter- First is the high degree of specificity in the organiza- ventions designed to maximize recovery by driving tion and processing of information. Specialized and shaping neural reorganization. sensory receptors, modality-specific line of commu- The focus of this chapter will be on loss of somatic nication (Gardner and Martin, 2000), specific colum- sensations, treatments currently available to address nar organization and sub-modality-specific neurons this problem, and the potential application of theo- in primary (SI) and secondary (SII) somatosensory ries of perceptual learning and neural plasticity. areas (Mountcastle, 1997) support this specificity. More detail will be given to therapies following cen- Second, the opportunity for convergence of somato- tral nervous system (CNS) lesions, with particular sensory information within the CNS (Mesulam, reference to stroke. Comparisons will also be made 1998), as well as the presence of distributed sensory in relation to loss following peripheral nervous system networks and multiple somatotopic representation (PNS) lesions. (Gardner and Kandel, 2000), impact on the scope for neural plastic changes and rehabilitation outcome.

16.1 Nature of impairment and functional implications of loss Loss of somatic sensation following interruption to central and peripheral Definition and processing within the nervous systems somatosensory system Loss of somatic sensations can be sustained due to Somatosensory function is the ability to interpret damage at various levels of the sensory system, for bodily sensation (Puce, 2003). Sensory systems are example from receptors to peripheral nerves, spinal organized to receive, process and transmit informa- cord, brainstem and cerebral cortex. This may result tion obtained from the periphery to the cerebral from disease or trauma associated with a wide range cortex. Within the somatosensory system submodal- of conditions (see Section E Disease-specific ities of touch, proprioception, temperature sense, Neurorehabilitation Systems of Volume II). Somato- pain and itch are identified. (Gardner and Martin, sensory impairment may be in the form of anesthe- 2000). Detailed description of the system involved sia (total loss of one or more sensory submodalities in sensory processing is provided in seminal texts in the region), hyposensitivity (reduced ability to

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perceive sensations, including poor localization, of an object without crushing or dropping it, using discrimination and integration), or hypersensitivity cutlery, fastening buttons, writing and walking on (non-noxious stimuli become irritating, for exam- uneven ground become difficult and often frustrat- ple dyesthesia, paraesthesia or causalgia). Clinical ing (Carey, 1995). The important role of sensation in description of loss should include identification of motor function is particularly evident in: control of body part and submodalities affected as well as the pinch grip (Johansson and Westling, 1984); ability to level of processing impairment, for example detec- sustain and adapt appropriate force without vis- tion, discrimination and integration of information ion (Jeannerod et al., 1984); object manipulation across submodalities. (Johansson, 1996); combining component parts of There are differences in the nature of the loss fol- movement such as transport and grasp (Gentilucci lowing peripheral and CNS lesions. For example, et al., 1997); discrimination of surfaces at end of hand- injury to the PNS involves well-defined loss of spe- held objects (Chan and Turvey, 1991); restraint of cific modalities that can be mapped relative to the moving objects (Johansson et al., 1992); and adjust- nerve distribution or receptor location. In compari- ment to sensory conflict conditions such, as a son, loss following CNS lesions such as stroke can rough surface (Wing et al., 1997). Moreover, the result in very different patterns of deficit, from com- affected limb may not be used spontaneously, plete hemianaesthesia of multiple modalities to despite adequate movement abilities. This may dissociated loss of sub-modality specificity in a par- contribute to a learned non-use of the limb and ticular body location (see Carey, 1995 for review). further deterioration of motor function after stroke Loss of discriminative sensibilities is most charac- (Dannenbaum and Dykes, 1988). These activity teristic (Bassetti et al., 1993; Carey, 1995; Kim and limitations impact on life roles, social communica- Choi-Kwon, 1996), thresholds for primary sensory tion, safety and participation in personal and domes- qualities (e.g., touch) are often indefinable (Head tic activities of daily living as well as sexual and and Holmes, 1911–1912), qualitative alterations, leisure activities (Carey, 1995). response variability (Carey, 1995) and dissociated The personal and functional implications of sen- sensory loss (Roland, 1987; Bassetti et al., 1993) are sory loss are highlighted in the words of a client who observed, and hypersensitivity may be present ini- experienced sensory loss after stroke: “… my right tially or develop over time (Holmgren et al., 1990). side cannot discriminate rough, smooth, rigid or Typically the loss is contralateral to the injury, malleable, sharp or blunt, heavy or light. It cannot although ipsilateral deficits are also reported (Carey, tell whether that which touches it as hand or tennis 1995; Kim and Choi-Kwon, 1996). The early and racket…it is frustratingly difficult to control or feel chronic pattern of deficit may be influenced by the relaxed about any right-sided movement … . How site of lesion, relative sparing and redundancy within does one trust a foot that “feels” as though it has no the distributed sensory system and neural plastic real connection with the earth? It is difficult to pick changes that may occur with recovery. up or hold a pair of glasses or a sheet of paper when one’s right hand/fingers feel uncontrollably strong and very big and clumsy, capable of crushing objects Functional implications of loss with one’s grip yet incapable of letting go or throw- Impairment of body sensations poses a significant ing off even the lightest objects (e.g. a tissue). … loss in its own right and has a negative impact on better to feel something-however bizarre-than effective exploration of the environment, personal nothing.” safety, motor function, and quality of life (Rothwell Loss of somatic sensations also negatively impacts et al., 1982; Carey, 1995). Everyday tasks such as on rehabilitative and functional outcomes, as indi- searching for a coin in a pocket, feeling if a plate is cated in a review of stroke outcome studies (Carey, clean when washing dishes, maintaining the grip 1995). It has a cumulative impact on functional Selzer 2-16.qxd 05/09/2005 15:09 Page 233

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deficits beyond severity of motor deficits alone “normal”, “impaired” or “absent” (Wade, 1992), have (Patel et al., 2000) and negatively impacts on reac- variable reliability (Winward et al., 1999), no defined quisition of skilled movements of the upper limb criterion of abnormality, and are often insensitive or (Kusoffsky et al., 1982; Jeannerod et al., 1984), pos- inaccurate (Carey et al., 2002c). Kim and Choi-Kwon tural control and ambulation (Reding and Potes, found that discriminative sensation remained in 1988). The importance of the sensory system as an only 3 of 25 stroke patients who were reported as early indicator of motor recovery after stroke has having no sensory impairment on the basis of con- been suggested in neuroimaging (Weiller, 1998) and ventional sensory tests (Kim and Choi-Kwon, 1996). clinical (Kusoffsky et al., 1982) studies. It has been Over the past decade new measures have been suggested that sensory reorganization may precede developed for use post-stroke. Clinical test batteries motor reorganization and may, in fact, trigger the developed are the Nottingham Sensory Assessment latter (Weiller, 1998). (NSA) (Lincoln et al., 1991; Lincoln et al., 1998) and the Rivermead Assessment of Somatosensory Performance (RASP) (Winward et al., 2002). The RASP is standardized, uses seven quantifiable sub- 16.2 Assessment of somatic sensation tests of touch and proprioceptive discrimination and includes three new instruments, the neurome- Guidelines for the selection of ter, neurotemp and two-point neurodiscriminator. measures for use in clinical settings Intra and inter-rater reliability are high (r 0.92). The directive to follow evidence-based practice The NSA employs methods consistent with clinical demands that clinicians employ quantitative meas- practice, but are more detailed and standardized. ures that are valid and reliable. Numerous tests have Intra and inter-rater reliability are variable, with been developed to evaluate the various qualities of most tests showing relatively poor agreement across sensibility, including touch, pressure, temperature, raters. The revised NSA reports acceptable (k 0.6) pain, proprioception and tactual object recognition agreement in only 12 of 86 items (Lincoln et al., 1998), (Carey, 1995; Dellon, 2000). In clinical settings we and inter-rater reliability of 0.38–1.00 for the stereog- need information not only on thresholds of detec- nosis component (Gaubert and Mockett, 2000). tion, but also on the ability to make accurate dis- New tests of specific sensory functions commonly criminations and recognize objects with multiple impaired post-stroke have also been achieved. A test sensory attributes. Selection of suitable measures of sustained touch-pressure, based on the need to should be based on the following criteria: valid appreciate sustained contact of an object in the hand measurement of the sensory outcome of interest, during daily manual tasks, was developed and impair- for example discrimination; quantitative measure- ment demonstrated in six patients with severe ment; objectively defined stimuli; control for test sensory deficit (Dannenbaum and Dykes, 1990). bias and other clinical deficits; standardized proto- Empirical foundations for the test are required. New col; adequate scale resolution to monitor change; measures of tactile (Carey et al., 1997) and proprio- good reliability and age-appropriate normative ceptive (Carey et al., 1996) discrimination provide standards. For a critique of routine clinical and quantitative measurement of the characteristic dis- quantitative measures refer to Carey (1995), Dellon criminative loss post-stroke. They are founded on (2000) and Winward et al. (1999). strong neurophysiological and psychophysical evi- The need for standardized measures for use fol- dence (Clark and Horch, 1986; Darian-Smith and lowing stroke has been highlighted (Carey, 1995; Oke, 1980; Morley, 1980) and perception of the grid Winward et al., 1999). Measures commonly used are surfaces has been associated with cerebral activa- largely subjective, lack standardized protocol (Lincoln tion in multiple somatosensory areas in unimpaired et al., 1991; Carey, 1995;), use gross scales such as (Burton et al., 1997) and impaired (Carey et al., 2002a) Selzer 2-16.qxd 05/09/2005 15:09 Page 234

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humans. The measures are quantitative, reliable, comparison, few studies have systematically inves- standardized, measure small changes in ability, have tigated the natural history of spontaneous recovery empirically demonstrated ability to differentiate of somatosensations post-stroke. Improvements have impaired performance relative to normative stan- been reported across a range of measures including dards (Carey et al., 1996, 1997) and advance current touch detection, texture and proprioceptive dis- clinical assessment (Carey et al., 2002c). Tests of fab- crimination and object recognition (see Carey, ric discrimination and discrimination of finger and 1995 for review). However, the extent of recovery is elbow position sense have also been developed varied (Kusoffsky et al., 1982), ranging from lasting (Carey, 1995) and are being empirically tested by us. deficits (Wadell et al., 1987) to “quite remarkable” In addition to quantitative measures of sensibility, improvement in capacities such as stereognosis it is important to evaluate the presence and impact (Schwartzman, 1972). The temporal aspects of recov- of the impairment in daily activities. This may ery are also relatively unknown. Recovery appears involve structured interview and/or observation of most marked within the first 3 months (Newman, occupational performance difficulties in tasks rele- 1972), although ongoing recovery has been observed vant to the patient. Focus of observations may at 6 months and later (Kusoffsky, 1990). It has been include impact of loss on unilateral and bilateral suggested that persistent deficit may be associated tasks, level of independence, nature of difficulties with particular lesion site (Corkin et al., 1970). (e.g., clumsy) and use of compensatory techniques. Tasks with varying sensory demands may be struc- Evidence of training-induced recovery tured to systematically assess the impact of sensory Evidence of training-induced sensory improvements loss. As yet there is no standardized test of the impact further highlights the potential for recovery following of sensory loss on daily activities. PNS (Dellon, 2000) and CNS (Carey, 1995) lesions. Moreover, improvements have been observed months and years post-injury, after the period of expected 16.3 Potential for recovery nerve regeneration (Dellon, 2000). Dellon (2000) asserts that results of sensory rehabilitation must be The potential for recovery of somatosensory abili- due to higher CNS functions and that cortical ties has been demonstrated, following lesions to plasticity is the underlying mechanism. Similarly peripheral (Dellon, 2000) and central (Carey, 1995) following stroke, task-specific and generalized train- nervous systems under both spontaneous and ing effects have been observed across tactile, pro- training-induced recovery conditions. prioceptive and object recognition tasks, under quasi-experimental and controlled conditions (see The natural history of recovery Section Review of documented programs in relation to basic science and empirical foundations of docu- The potential for recovery depends on regeneration mented of this chapter for review). In most instances of structures within the somatosensory system as the improvements have been observed after the well as the capacity for neural plasticity and reinter- period of expected spontaneous recovery. Neural pretation of altered stimuli. These factors are further plastic changes have also been proposed as the influenced by the level at which the system is inter- likely mechanism underlying these improvements. rupted, extent of injury, progression of disease, age, prior and intervening experience (Callahan, 1995; Neural plastic changes associated with recovery Carey, 1995; Dellon, 2000; see also Chapters 12, 13, of somatic sensations and 27 of Volume II). Regeneration and recovery following damage to PNS has been relatively Neural plastic changes occur in response to injury, but well described (Callahan, 1995; Dellon, 2000). In also as part of normal learning and development (refer Selzer 2-16.qxd 05/09/2005 15:09 Page 235

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to Section A on Neural plasticity in Volume I). The positive and negative patterns of brain reorganization cellular, physiological and behavioral mechanisms can occur and that these can be “strongly influenced operating in adaptive brain plasticity are discussed in by appropriate rehabilitation programs after brain this section. Changes can occur immediately post- damage” (Nudo et al., 1996b; Nudo, 1999). Brain lesion or months and years later and can involve mul- plasticity related to treatment-induced motor recov- tiple levels of the somatosensory system (Jones and ery has been suggested in the sensorimotor system Pons, 1998). Longer-term stable changes, likely linked of humans post-stroke (Liepert et al., 2000; Nelles with change in synaptic connections and learning, are et al., 2001; Carey J.R. et al., 2002). In addition, we have the most relevant for rehabilitation. Investigations in recently demonstrated good clinical recovery and humans confirm reorganization in somatosensory changes in ipsilesional SI, bilateral SII and premotor regions following extensive use (Pascual-Leone and areas following somatosensory training in a patient Torres, 1993), transient anesthesia (Rossini et al., 1994) who showed poor spontaneous recovery in the 6 and injury to the PNS (Merzenich and Jenkins, 1993) months prior (see Fig. 16.1, Patient 2). Investigation and CNS (Carey et al., 2002a; Wikström et al., 2000; see of changes in brain activation associated with train- also Chapters 12, 13 and 27 of Volume II). ing-induced recovery of somatosensations under Studies of change in human brain activation, sug- randomized control conditions is now required. gestive of neural reorganization, are providing new insights into the mechanisms underlying stroke 16.4 Approaches to retraining impaired recovery (Weiller, 1998; see also Chapter 5 of Volume sensory function II). Evolution of change over time and a potential relationship with recovery has been demonstrated Review of documented programs in relation to in the motor system (e.g., Carey et al., 2005; Small basic science and empirical foundations et al., 2002; Ward et al., 2003). Findings indicate involvement of cortical and subcortical sites primarily Neurorehabilitation needs to be founded on a rigor- within the pre-existing motor network and include ous basic and clinical science platform and include recruitment of sites not typically used for the task cure in its mission (Seltzer, introduction to this text). and return to a more “normal” pattern of activation. Sensory re-education has been an integral part of Changes in SI (Rossini et al., 1998; Wikström et al., the rehabilitation of patients with peripheral nerve 2000), SII (Carey et al., 2002a) and thalamus (Ohara disorders for many years. Some of the most influen- and Lenz, 2001) have been reported in the few stud- tial programs are those developed by Wynn Parry ies of somatosensory recovery post-stroke. In serial and Salter (1976) and expanded by Dellon (1981; pilot functional magnetic resonance imaging (fMRI) 2000). These programs employ principles of direct, studies we found re-emergence of activation in repeated sensory practice, feedback through vision, ipsilesional SI and bilateral SII in a stroke patient subjective grading of stimuli such as texture and who had marked sensory loss followed by good objects, verbalization of sensations and comparison recovery (Fig. 16.1, Patient 1; Carey et al., 2002a). In of sensations experienced across hands. Evidence comparison, only very limited recruitment in non- for the effectiveness of sensory training following primary sensory areas was observed in the second peripheral lesions is reviewed in (Dellon, 2000, patient who showed poor spontaneous recovery. Chapter 11). Whilst some programs are directed to As yet little is known about neural mechanisms localized somatosensory deficits and regeneration of underlying functional recovery associated with specific nerve fibers, Dellon (2000) highlights the specific training post-stroke in humans. Animal mod- need to focus on interpretation of altered stimuli at a els highlight the benefit of experience in facilitating cortical level based on evidence of neural plasticity. brain reorganization within motor and sensory sys- There are a relatively limited number of docu- tems. Controlled studies in primates suggest that both mented sensory retraining programs designed for Selzer 2-16.qxd 05/09/2005 15:09 Page 236

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Stroke Spontaneous recovery Patient 1 R hand 2 weeks 3 months 6 months CS SI

SII

Spontaneous recovery Training Patient 2 L hand 5 weeks 3 months 6 months 7.5 months

SI CS

SII

Left

Figure 16.1 Serial fMRI pilot studies of touch discrimination during the interval of spontaneous recovery (non-specific rehabilitation) and following specific sensory retraining post-stroke. The functional echoplanar axial slices shown sample two brain regions of interest, that is primary somatosensory cortex (SI) posterior to the central sulcus (CS), and secondary somatosensory cortex (SII). Significant brain activation (Puncorrected 0.0001) in ipsilesional SI and bilateral SII observed during stimulation of the affected hand is circled.

use with stroke patients (Carey, 1995). Early studies neurophysiologic concepts and “rules governing suggesting improvement of sensory abilities somatosensory cortical reorganization after trauma”. (Vinograd et al., 1962; De Jersey, 1979) have lacked Their program involved stimulation of “important controls and a sound theoretical basis. The program sensory surfaces” at an intensity sufficient for by Vinograd et al. involved repeated exposure to test appreciation and in a task that was motivating to the stimuli with 3D feedback from a box lined with mir- patient. Subjects were encouraged to attend to the rors while DeJersey used bombardment with multi- input and given reinforcement. Electric stimulation ple sensory stimuli. The only early study with a and velcro were used in the early stages, followed by controlled design (Van Deusen Fox, 1964) also did finger localization, exploration of velcro shapes and not employ current theories of perceptual learning use of utensils taped with velcro. Improvement was and neurophysiology and failed to obtain a thera- reported in the case study presented. peutic effect (see Carey, 1995 for review). Yekutiel and Guttman (1993) reported significant In comparison, Dannenbaum and Dykes (1988) gains following sensory retraining in 20 stroke described a therapeutic rationale based on patients with chronic sensory impairment under Selzer 2-16.qxd 05/09/2005 15:09 Page 237

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controlled conditions. Principles of training were ten or fewer training sessions and maintained over derived initially from peripheral nerve injury train- follow-up periods of 3–5 months, suggesting a long- ing programs (Wynn Parry and Salter, 1976), with term therapeutic effect. SST effects were specific to contributions from psychology (Yekutiel, 2000). The the trained sensory perceptual dimension (tactile or essential principles included focus on the hand, proprioceptive) and stimulus type (e.g., texture grat- attention and motivation, guided exploration of the ings or fabrics). Generalized improvements in touch tactics of perception and use of the “good” hand. discrimination, that is untrained fabric surfaces, The findings confirm that sensory discriminations were achieved by the program deliberately oriented are trainable after stroke and suggest a potential for to enhance transfer (Carey and Matyas, 2005), as generalized sensory gains. The authors reported shown in Fig. 16.2. Meta-analysis of SST effects variation in results across patients and noted that, (tactile z 8.6, P 0.0001; proprioception “the method used – although aimed at higher brain z 4.3, P 0.0001) and SGT effects (tactile centers – may still be too “peripheral” (Yekutiel and z 5.7; P 0.0001) supports the overall conclu- Guttman, 1993) (p. 243). sion that tactile and proprioceptive discriminations We have developed and investigated the effective- are retrainable following stroke and that both ness of two different approaches to training sensory modes of training are effective. Finally, we have also discrimination: Stimulus Specific Training (SST) applied the SGT approach to training friction dis- (Carey, 1993; Carey et al., 1993) and Stimulus Gener- crimination and investigated its effect on the funda- alization Training (SGT) (Carey and Matyas, 2005). mental pinch grip task in pilot studies, with positive The programs employ principles derived from theor- results (Carey et al., 2002b) ies of perceptual learning (Gibson, 1991; Goldstone, Two further retraining programs have been docu- 1998), recovery following brain damage (Bach-y- mented recently. These programs are in part derived Rita, 1980; Weiller, 1998) and neurophysiology of from earlier programs, employ principles consistent somatosensory processing (Gardner and Kandel, with perceptual learning and neural plasticity and 2000). SST was designed to maximize improvement focus on training sensory and motor functions. in specific stimuli trained. It involves repeated pres- Smania et al. (2003) describe a program of sensory entation of targeted discrimination tasks; progres- and motor exercises for patients with pure sensory sion from easy to more difficult discriminations; stroke. The program involved graded exercises, attentive exploration of stimuli with vision occluded; reported to be challenging for the patient, and feed- use of anticipation trials; feedback on accuracy, back on accuracy and execution of task for each method of exploration and salient features of the trial. Exercises focused on tactile discrimination using stimuli; and use of vision to facilitate calibration of different textured surfaces, object recognition, joint sensory information (Carey, 1993; Carey et al., 1993). position sense, weight discrimination, blindfolded In comparison, the SGT approach was designed to motor tasks involving reach and grasp of different facilitate transfer of training effects to untrained, objects, as well as practice of seven daily life activi- novel stimuli and included additional principles of ties. Improvement in sensory and motor outcomes, variation in stimulus and practice conditions, inter- as well as increased use of the affected arm in daily mittent feedback and tuition of training principles activities, was reported in the four cases studied. (Carey and Matyas, 2005; Gibson, 1991; Schmidt and Byl et al. (2003) described a program aimed to Lee, 1999). improve accuracy and speed in sensory discrimina- SST effects were replicated in 37 of 41 time-series tion and sensorimotor feedback. Principles, derived across 30 single-case experiments. Stimulus Gener- from studies of neural adaptation, included: match- alization effects were found in 8 of 11 time-series ing tasks to ability of the subject, attention, repeti- across 11 subjects. Marked improvements, to within tion, feedback on performance and progression in normal performance standards, were achieved within difficulty. Sensory training focused on improving Selzer 2-16.qxd 05/09/2005 15:09 Page 238

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Phase 1Phase 2 Phase 3 sensory discriminations through games and fine 4 motor activities, use of velcro on objects, retrieving 3.5 Baseline objects from a box filled with rice and exercises in 3 2.5 graphesthesia, localization, stereognosis and kines- 2 thesia. Movements of the hand, mental rehearsal to 1.5 reinforce learning and tasks to quiet the nervous sys- 1 tem were also used. Patients were educated regard- 0.5 Stimulus Stimulus ing the potential for improvement in neural 0 specific generalization processing and the unaffected hand was constrained Trained grid matching score Z 0.5 training training 1 through wearing of a glove. Training was investigated

3.5 in 21 subjects with order of sensory or motor training 3 crossed, although no placebo intervention period 2.5 was employed. Improvements in sensory discrimi- nation, fine motor function and musculoskeletal 2 measurements of the upper limb were reported fol- 1.5 lowing sensory training. Gains were hemispheric 1 and training specific. 0.5 In summary, recent training programs with suc- Untrained grid matching score Z 0 cessful outcomes have included a number of com-

3.5 mon principles consistent with theories of learning 3 Extended baseline and neural plasticity. These include: attention to the 2.5 sensory stimulus; repetitive stimulation with and

2 without vision; use of tasks that are challenging and motivating; focus on the hand; graded progression 1.5 of tasks and feedback on accuracy and execution. A 1 more detailed discussion of principles of training 0.5 related to perceptual learning and neural plasticity

Untrained fabric matching score Z 0 follows with suggestions for their application. 0 51015202530 Session

Figure 16.2 Example single-subject case chart demonstrating 16.5 Principles of neural plasticity and SST effects on trained grids and untrained grids. Improvement learning as they apply to rehabilitation in untrained fabric discriminations is evident only following introduction of the program designed to enhance of sensation generalization. Baseline conditions of repeated exposure to the stimuli were not sufficient to effect clinically significant Identification and application of principles to improvement. The raw time-series data ( ) and predicted time- optimize perceptual learning and brain series models ( ) are shown. Higher scores represent an adaptation improvement in texture matching ability. The criterion of normality for the Grid Matching Test is 0.62 z score Evidence of neural plasticity provides a strong foun- (mean 1.47) and for the Fabric Matching Test is 1.61 z score dation for restorative sensory retraining post-injury, (mean 2.46). Statistical time-series analyses of trend and both in acute and chronic phases. Review of theor- level effects (P 0.01) confirm the training effects shown for ies of perceptual learning and the conditions under this subject. which neural plastic changes occur suggests a number of principles that have potential application in retrain- ing somatosensations following PNS or CNS injury. Selzer 2-16.qxd 05/09/2005 15:09 Page 239

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Table 16.1. Summary of principles of sensory training derived from theories of perceptual learning, neural plasticity and physiology of the somatosensory system.

Derived from and/or consistent with theories of

Principle of training Perceptual learning Neural plasticity Physiology

Repeated stimulation improvement maximal modification of sensory specificity of processing of specific stimuli for specific stimulus map is task-dependent within the system Attentive exploration attention important modulation of component of sensory in learning neural plasticity processing Vision occluded force use of vision may dominate somatosensory system Motivating/ link with attention, brain responds to meaningful task learning and success meaningful goals Use of anticipation activation of similar consistent with trials (and imagery) sites as for direct normal processing stimulation. Feedback on extrinsic and summary enhance new – accuracy feedback may enhance connections – method of exploration learning and summary feedback Calibration of sensation: improved perception cross-modal plasticity pre-existing connections within and across modalities within system Progression from easy to required for learning progressively more difficult discriminations within and across sensory challenge system dimensions Intensive training improved performance forced use, and retention competitive use Variation in stimuli, facilitates transfer of intermittent feedback and training effects tuition of training principles

Most of the principles identified from these fields are et al., 1996a) and the system is competitive complementary, consistent with the knowledge that (Merzenich and Jenkins, 1993; Weinreich and neural plasticity underlies learning and recovery fol- Armentrout, 1995). Functional reorganization has lowing injury. In addition, the physiology of process- been demonstrated after behaviorally controlled ing somatosensory information must be considered tactile stimulation in intact animals (Recanzone in application to the sensory system. More recent et al., 1992). Forced use of the system, for example sensory retraining approaches have begun to base using constraint induced movement therapy, has their training on these principles (see Section Review also been associated with neural plastic changes in of documented programs in relation to basic science post-stroke motor recovery (Liepert et al., 2000). and empirical foundations of this chapter for review). Even less intensive programs based on principles Key principles that have been successfully applied, or of motor learning found training-induced changes have potential for application, are discussed below. (Carey J.R. et al., 2002). Importantly, repetitive use Their application is summarized in Table 16.1. alone may not be sufficient to effect changes in Neural plastic changes are experience-dependent cortical representation. Rather changes are associ- (see Section A on Neural plasticity in Volume I; Nudo ated with specific skill learning, consistent with a Selzer 2-16.qxd 05/09/2005 15:09 Page 240

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“learning-dependent” hypothesis of neural plastic- increasing the attention paid to important features ity (Karni et al., 1995; Plautz et al., 2000). Sensory (with less noticing of irrelevancies) (Gibson, 1969; neurorehabilitation should therefore challenge the Goldstone, 1998). Perceptual learning (Goldstone, sensory system using repeated stimulation of tar- 1998) and neurophysiological (Johnson and Hsiao, geted sensory tasks coupled with an intensive percep- 1992) evidence propose that “distinctive features of tual-learning based training program. difference” are learned and form the basis of transfer Learning is reported to be maximal for the specific of training. Attention is also important in the modu- task trained (Gibson, 1969; Goldstone, 1998; Sathian lation of cortical plasticity (see Chapter 11 of Volume and Zangaladze, 1997), consistent with highly spe- II), particularly in early stages of plastic changes and cific organization of the system (see Section learning (Karni et al., 1995). Thus patients should Definition and processing within the somatosen- actively (where possible) and purposively explore sory system of this chapter for review) and evidence sensory stimuli with attention directed to distinctive that functional reorganization is directly linked with features of difference. This may be facilitated through changes in cortical regions engaged by these inputs requiring a response and guiding the patient to (Recanzone et al., 1992). Repetition over time with search for distinctive features (Carey et al., 1993). an increasing number of coincident events serves to Further, as vision may dominate tactile and proprio- strengthen synaptic connections (Byl and Merzenich, ceptive senses in some instances (Clark and Horch, 2000). However, competition between afferent inputs 1986; Lederman et al., 1986), exploration of stimuli for connections in the sensory cortex (Merzenich and with vision occluded should be included to allow Jenkins, 1993) suggests the need for caution with over- subjects to focus specifically on the somatic sensa- stimulation of a specific site at the expense of related tions (Carey et al., 1993). areas. Consequently to maximize task-specific learn- Anticipation may facilitate recruitment of existing ing, training stimuli and the method of processing or new sensory sites in the brain. Similar brain sites the information should match targeted discrimina- are active under direct stimulation and anticipated tion tasks (Carey et al., 1993). Training of important stimulation conditions (Roland, 1981). Further, prior sites normally responsible for the sensation, for and subjective experience can influence early stages example the hand (Dannenbaum and Dykes, 1988; of information processing and facilitate stimulus Yekutiel and Guttman, 1993), and discriminations differentiation (Goldstone, 1998). Anticipation tri- characteristically impaired and important for daily als, in which the patient is informed that a limited function (Carey et al., 1993) have been recommended. set of previously experienced stimuli will be used Motivation is important in learning (Goldstone, (Carey et al., 1993), may tap into this capacity and 1998) and recovery after brain injury (Bach-y-Rita, encourage new neural connections. A patient may 1980), and the brain responds to meaningful goals also be encouraged to imagine what a stimulus (Nudo et al., 1996b). Training should therefore be should feel like, based on evidence that haptic (tac- goal directed, interesting and demanding if it is to tile and proprioceptive) information is represented tap into the brain’s potential for functional reorgan- through imagery (Klatzky et al., 1991). ization (Byl and Merzenich, 2000; Yekutiel, 2000). Augmented feedback on accuracy of response It should provide regular opportunities for success, outcome and on performance is important in with reinforcement to encourage motivation and skill acquisition (Schmidt and Lee, 1999) and participation (Carey, 1993; Yekutiel, 2000). may enhance perceptual learning (Gibson, 1969). Attention is crucial in perceptual learning. Attentive Although improvement in perceptual discriminations exploration of stimuli allows purposeful feedback may be experienced in unimpaired subjects without within the sensory-perceptual system (Epstein et al., extrinsic feedback in some cases (Epstein et al., 1989) and perception becomes adapted to tasks by 1989), practice with correction can enhance learning Selzer 2-16.qxd 05/09/2005 15:09 Page 241

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(Gibson, 1969). We found that repeated exposure Specificity of learning and principles alone was insufficient to effect a positive training to facilitate learning transfer outcome in the majority of cases post-stroke (Carey Whilst the above principles have been associated et al., 1993; Carey and Matyas, 2005). Thus feedback with positive perceptual learning, there are limits on on accuracy of response and performance, for exam- the generality of perceptual learning. Perceptual ple method of exploration (Lederman and Klatzky, learning is usually highly specific to the task, recep- 1993), should be provided. Feedback should be tor location and method of processing (Sathian and immediate, precise and quantitative to maximize Zangaladze, 1997; Goldstone, 1998). Similarly, we acquisition (Salmoni et al., 1984). Summary feedback found highly specific training effects in tasks also enhances learning (Salmoni et al., 1984) and employing the same sensory dimension (tactile or should be provided at the end of each training session. proprioceptive), sub-modality (grid or fabric tex- Calibration of perceptions would also appear to tures) and body location (fingertip or wrist) with be important. This may involve comparison of the SST post-stroke (Carey et al., 1993; Carey and sensation with the other hand (Gibson, 1969) and Matyas, 2005). However, perceptual transfer is pos- use of vision to facilitate cross-modal calibration sible in some instances with unimpaired subjects (Lederman et al., 1986), consistent with activity in (Epstein et al., 1989; Ettlinger and Wilson, 1990; visual cortical regions during tactile perception Spengler et al., 1997). Similarity between original (Zangaladze et al., 1999). Computational neural and transfer tasks is an important factor influencing models indicate that when two modalities are the degree of transfer (Gibson, 1969). It has been trained at the same time and provide feedback for suggested that transfer should be more prominent each other, a higher level of performance is possible where the stimuli are more complex and potentially than if they remained independent (Becker, 1996). share a number of distinctive features (Gibson, Moreover, cross-modal plasticity in sensory systems 1991; Goldstone, 1998). Transfer across body sites (see Chapter 10 of Volume II) may facilitate alternate has also been reported in unimpaired systems and new neural connections. (Sathian and Zangaladze, 1997; Spengler et al., 1997), Finer perceptual differences are able to be distin- and may be influenced by the attention demands guished through exposure to a series of graded stim- and complexity of the task (Ahissar and Hochstein, uli (Ahissar and Hochstein, 1997; Goldstone, 1998). 1997). Graded progression facilitates perceptual differenti- Principles of learning that facilitate transfer of ation, especially of complex stimuli, as presentation training effects in unimpaired subjects have potential of an easy discrimination first allows the subject application following injury. Transfer of training to allocate attention to the relevant dimension effects is more effective when variation in stimuli is (Goldstone, 1998). Further, transfer from one stimu- employed (Gibson, 1991; Goldstone, 1998; Schmidt lus to another within a unidimensional sensory qual- and Lee, 1999). Optimally this should include training ity requires presentation in a graded manner (Gibson, across a variety of stimuli with a wide range of dis- 1969). Thus training should progress from easy to tinctive features, for example roughness characteris- more difficult discriminations across stimuli and tics, as well as variation in tasks and environments within a unidimensional sensory quality. (Carey and Matyas, 2005). To achieve grading, pro- Performance is better on frequently presented gressive difficulty should be defined across stimuli items than rare items (Allen and Brooks, 1991). In sets as well as within sets (Carey and Matyas, 2005). addition, best available evidence suggests that train- Intermittent feedback on accuracy of response ing should continue for some time after “mastery” to (Winstein and Schmidt, 1990) and specific instruc- increase retention (Lane, 1987). This further suggests tion on principles of training and how these apply the need for repetition and intensive training. Selzer 2-16.qxd 05/09/2005 15:09 Page 242

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across tasks (Cormier and Hagman, 1987) have also training-induced recovery is associated with been associated with enhanced transfer and reten- changes in the functional neuroanatomy of sensa- tion. Further, an important part of learning transfer tion in humans. In particular it is unknown whether tasks is acquiring the capacity to cope with novel sites different to those typically used are involved in situations (Schmidt and Lee, 1999). This suggests the recovery process, possibly suggestive of different the need to provide exposure to novel stimuli with behavioral strategies. Clinically effective sensory opportunity to get feedback on the act of generaliza- training programs, derived from theories of percep- tion (Carey and Matyas, 2005). tual learning and recovery following brain damage, In summary, positive findings from studies of sen- may be used to test for outcomes related to brain sory retraining (see section Review of documented adaptation. Confirmation of the prediction that programs in relation to basic science and empirical neural plastic changes occur primarily within the foundations of this chapter for review) support the pre-existing somatosensory system (Weinreich and application of principles of training derived from lit- Armentrout, 1995), will highlight the importance of erature on perceptual learning and neural plasticity. sparing and dynamic adaptation within pre-existing Further, the nature of training, that is stimulus spe- sensory sites. Evidence of recruitment of different cific versus generalization optimized, appears cru- sites may identify involvement of other systems cial to outcome. Evidence of a learning phenomenon important in recovery, such as attention (see associated with sensory retraining post-stroke has Chapter 11 of Volume II) and visual (see Chapter 10 been quantified in the intervention time-series data of Volume II) systems. This will advance our under- of our patients (Carey, 1993; see also Fig. 16.2). The standing of whether training is operating at a level of improvement curve was consistent with that restitution or substitution within the system and described in the learning literature (Lane, 1987; provide insight into behavioral strategies associated Epstein et al., 1989) and in studies of neural plasticity with training. Comparison with motor recovery (Recanzone et al., 1992). However, in contrast to findings will help determine if there is a common unimpaired subjects (Epstein et al., 1989), the char- model of neural plasticity associated with motor acteristic learning curve was only achieved under and somatosensory recovery. supervised training conditions (Carey et al., 1993). Systematic investigation of the conditions under The potential for generalization of training within a which behavioral improvement and neural repair is sensory dimension has also been demonstrated most effectively achieved is required to provide ongo- post-stroke, provided a program designed to ing direction for the development of science-based enhance transfer is used (Carey and Matyas, 2005). interventions. For example, the timing (post-injury) Other programs that have employed training across and intensity of training requires investigation, given a variety of tasks have also found generalized train- evidence of possible maladaptive changes (Merzenich ing effects (Byl et al., 2003; Smania et al., 2003; and Jenkins, 1993; Nudo et al., 1996b). Investigation Yekutiel and Guttman, 1993). of the need for specific training, compared to non- specific exposure, and the neural outcomes of learn- ing transfer (Spengler et al., 1997) will help elucidate 16.6 Future directions for the integration the mechanisms and brain regions involved in differ- of basic science in clinical practice, as ent training methods. Similarly, different principles applied to neurorehabilitation of somatic of training (e.g., cross-modality matching and feed- sensation back on accuracy) require systematic investigation of their contribution as they may involve different neu- Brain networks may reorganize to optimize stroke ral structures and mechanisms. Paradigms that per- recovery. However, despite evidence of behavioral mit investigation of component stages in neural improvement, it is not known to what extent processing need to be conducted and interpreted Selzer 2-16.qxd 05/09/2005 15:09 Page 243

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using models of analysis that focus on connectivity investigations of the relationship between sensation within the system. and other abilities, such as pinch grip, and the effect Knowledge of the relationship between brain acti- of improving sensation on motor function and vation and recovery will have predictive significance activities of daily living. in relation to identifying patients who are likely to show spontaneous recovery and/or who are able to benefit from training. Potential explanations for Acknowledgements individual differences in the nature and extent of recovery may relate to lesion site (Zemke et al., 2003) I wish to acknowledge the contribution of collabora- and remote changes in structure, including diaschi- tors who have worked with me on various aspects of sis (Seitz et al., 1999). Investigation of the associa- research related to sensory recovery and retraining tion between structural brain changes and the following stroke. In particular Ass/Prof Thomas brain’s capacity for reorganization is indicated. Matyas and Ms Lin Oke have collaborated on the Further development of current training programs clinical studies investigating methods of assessing is also indicated. Programs reviewed (see Section and training somatosensations post-stroke. Ongoing Review of documented programs in relation to basic clinical studies are being conducted also in collabo- science and empirical foundations of this chapter for ration with Prof Derek Wade and Dr Richard review) have incorporated principles consistent with Macdonnell. Investigation of neural outcomes asso- perceptual learning and neural plasticity. However, ciated with motor and sensory recovery under spon- individual features of the training protocols have not taneous and training-induced recovery conditions been dissected. This is necessary to identify the criti- is being conducted in collaboration with a number cally important elements associated with successful of researchers including Prof Geoffrey Donnan, learning and transfer. Previous studies have provided Dr David Abbott, Dr Gary Egan, Prof Aina Puce and some insight into the boundaries of spontaneous and Prof Rüdiger Seitz. facilitated transfer with stroke patients (Carey et al., 1993; Carey and Matyas, 2005). Investigation of simi- larity of trained and transfer tasks, method of infor- REFERENCES mation processing, level of task difficulty and relative Ahissar, M. and Hochstein, S. (1997). Task difficulty and the speci- body location on learning transfer is needed to guide ficity of perceptual learning. Nature, 387, 401–406. clinical training programs and clarify the nature of Allen, S.W. and Brooks, L.R. (1991). Specializing the operation of what is being learnt. an explicit rule. J Exp Psychol Gen 120, 3–19. The most optimal combination of principles may Bach-y-Rita, P. (1980). Brain plasticity as a basis for therapeutic also vary with individual patient characteristics procedures. In Recovery of function: theoretical considera- including the nature of loss (e.g., detection versus tions for brain injury rehabilitation (ed. Bach-y-Rita, P.), discrimination versus multisensory integration), pp. 225–263. Hans Huber, Vienna. the phase of recovery (acute versus chronic) and the Bassetti, C., Bogousslavsky, J. and Regli, F. (1993). Sensory syn- site of lesion (PNS versus CNS or specific location dromes in parietal stroke. Neurology, 43, 1942–1949. within these). Systematic investigation of these is Becker, S. (1996) Mutual information maximization: models of cortical self-organization. Network Comp Neural Syst, 7, 7–31. indicated. The focus of training could also be Burton, H., MacLeod, A.M., Videen, T.O. and Raichle, M.E. expanded to include training in discrimination of (1997). Multiple foci in parietal and frontal cortex activated size, shape and weight of objects, detection of slip by rubbing embossed grating patterns across fingerpads: a when holding objects, regulation of pressure during positron emission tomography study in humans. Cereb grasp and spontaneous use of the limb. Finally, the Cortex, 7, 3–17. ability to modify sensory abilities experimentally Byl, N., Roderick, J., Mohamed, O., Hanny, M., Kotler, J., Smith, opens up an experimental paradigm for future A., Tang, M. and Abrams, G. (2003). Effectiveness of sensory Selzer 2-16.qxd 05/09/2005 15:09 Page 244

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