Thomas Jefferson University Jefferson Digital Commons Department of Occupational Therapy Faculty Department of Occupational Therapy Papers

5-2010 Examining the evidence for sensory- driven : implications for sensory- based occupational therapy for children and adolescents. Shelly J. Lane Virginia Commonwealth University

Roseann C. Schaaf Thomas Jefferson University, [email protected]

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Recommended Citation Lane, Shelly J. and Schaaf, Roseann C., "Examining the neuroscience evidence for sensory-driven neuroplasticity: implications for sensory-based occupational therapy for children and adolescents." (2010). Department of Occupational Therapy Faculty Papers. Paper 23. http://jdc.jefferson.edu/otfp/23

This Article is brought to you for free and open access by the Jefferson Digital Commons. The effeJ rson Digital Commons is a service of Thomas Jefferson University's Center for Teaching and (CTL). The ommonC s is a showcase for Jefferson books and journals, peer-reviewed scholarly publications, unique historical collections from the University archives, and teaching tools. The effeJ rson Digital Commons allows researchers and interested readers anywhere in the world to learn about and keep up to date with Jefferson scholarship. This article has been accepted for inclusion in Department of Occupational Therapy Faculty Papers by an authorized administrator of the Jefferson Digital Commons. For more information, please contact: [email protected]. Examining the Neuroscience Evidence for Sensory- Driven Neuroplasticity: Implications for Sensory-Based Occupational Therapy for Children and Adolescents

Shelly J. Lane, Roseann C. Schaaf

KEY WORDS When Ayres first presented the theory of sensory integration (SI), she grounded it in the neuroscience lit-  evidence-based practice erature. Neuroplasticity was then, and is today, considered to be at the heart of this theory. This evidence- based review sought to critically examine the basic science literature to specifically identify evidence for the  feedback, sensory assumptions and tenets of Ayres’ theory of SI. We reviewed literature between 1964 and 2005, within  neuronal plasticity psychological, physiological, and biomedical areas, addressing neuroplasticity. The review focused on  occupational therapy sensorimotor-based neuroplasticity; explored the data that addressed the links among sensory input,  sensation function, and behavior; and evaluated its relevance in terms of supporting or refuting the theoretical premise  sensation disorders of occupational therapy using an SI framework (OT/SI) to treatment. Although direct application from basic science to OT/SI is not feasible, we concluded that there was a basis for the assumptions of Ayes’ SI theory.

Lane, S. J., & Schaaf, R. C. (2010). Examining the neuroscience evidence for sensory-driven neuroplasticity: Implications for sensory-based occupational therapy for children and adolescents. American Journal of Occupational Therapy, 64, 375–390. doi: 10.5014/ajot.2010.09069

Shelly J. Lane, PhD, OTR/L, FAOTA, is Professor and hat is the neuroscience evidence that occupational therapy using a sensory Chair, Department of Occupational Therapy, Assistant Wintegrative framework with children and adolescents will be effective? This Dean for Research, School of Allied Health Professions, Virginia Commonwealth University, 730 East Broad Street, question was designed to investigate the basic neural and developmental science Suite 2050, Richmond, VA 23219; [email protected] literature that might support or refute the use of occupational therapy using a sensory integration (OT/SI) frame of reference for treatment. Roseann C. Schaaf, PhD, OTR/L, FAOTA, is Associate Professor and Vice Chairman, Department of Occupational Therapy, Thomas Jefferson University, Statement of the Problem Philadelphia, PA. Participation in daily activities in part depends on the ability to process and integrate sensory information within the body and from the environment (Ayres, 1972; Bar-Shalita, Vatine, & Parush, 2008; Bundy & Murray, 2002; Gal, Cermak, & Ben-Sasson, 2007). A significant number of children experience difficulty processing and integrating sensory information. In fact, Ahn, Miller, Milberger, and McIntosh (2004) found that 5%–15% of children in the general population of kindergarten-age children demonstrate difficulties with sensory modulation. This number is estimated to be even higher in clinical populations; 80%–90% of children with autism spectrum disorders have been identified as showing atypical sensory responsivity (Rogers & Ozonoff, 2005; Tomchek & Dunn, 2007). OT/SI is one of the most frequently requested interventions by families of children with autism spectrum disorders (Green et al., 2006; Harrington, Rosen, Garnecho, & Patrick, 2006; Mandell, Novak, & Levy, 2005). OT/SI is based on the belief that engagement in individually tailored activities, rich in the needed sensory stimuli, will improve the ability of the brain and to process sensory information, enhance the orga- nization and integration of sensation, and, as a result, have a positive impact on the child’s ability to participate in daily life activities (Ayres, 1972, 1979).

The American Journal of Occupational Therapy 375 Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms In parallel with its popularity, OT/SI is a widely SI/sensory processing is the most investigated frame of criticized intervention framework (Miller, 2003; Shaw, reference in occupational therapy practice (Miller, 2003); 2002). Critics have cited insufficient direct empirical or most investigations of OT/SI have been clinically and clinical evidence to support the theoretical premise that behaviorally based. Although Ayres (1972) promoted SI improved processing and integration of sensory in- theory as one that linked brain and behavior, the mea- formation affects function and development in positive surement tools for investigating the basic tenets of the ways. Thus, the purpose of this article is to critically brain–behavior link in OT/SI, as well as the impact of examine the neuroscience literature for evidence to sup- OT/SI on specific brain function, have only recently been port or refute the potential benefit of OT/SI. In pre- realized. Thus, the scientific basis of OT/SI is currently paring this material, we focused on sensory-based grounded in animal research that explores the impact of neuroplasticity and explored the data in the neuroscience and single or multisensory literature that addressed the links among sensory input, inputs to the nervous system. As a result, this evidence- brain function, and behavior. We evaluated its relevance based investigation assumed a broad focus, largely outside in terms of supporting or refuting the theoretical premise the field of occupational therapy, and used animal and of the OT/SI framework. studies (as available) that investigated the effect of sensory experiences and input on nervous system struc- ture and function. We also examined literature that Background Literature linked sensory-based interventions to the performance of Occupational therapy using an SI framework is a widely used skills or occupational roles. This approach carried our intervention, primarily for children (see Ayres, 1972; Green literature search into the examination of interventions as et al., 2006; Harrington, Rosen, Garnecho, & Patrick, broad as environmental enrichment studies (e.g., 2006), but also applied to the adult population (Kinnealey placed in cages with varied toys and opportunities for & Fuiek, 1999; Kinnealey, Oliver, & Wilbarger, 1995; sensorimotor exploration; see Diamond, Rosenzweig, Pfeiffer & Kinnealey, 2003). Ayres’ (1972, 1979) SI theory Bennett, Lindner, & Lyon, 1972) and as focused as tactile postulated that adequate processing and integration of input to the finger tip (Ragert, Schmidt, Alternmu¨ller, & sensory information is an important foundation for adaptive Dinse, 2004). behaviors, where adaptive behaviors mean actions such as Our emphasis was on the multiple reflections of play and activities of daily living. Seven basic theoretical neuroplasticity or changes in the brain linked to changes in postulates form the foundation for the SI frame of reference environmental input or context. We examined studies for treatment (Bundy & Murray, 2002; see Schaaf et al., focused on both developmental and reactive neuro- 2009, for full listing of postulates). Several of the postulates plasticity, where developmental neuroplasticity refers to are regarding brain behavior functions. Pertinent to the those changes that take place in the course of typical topicweexaminedinthisreview,neuroplasticity, defined as development and reactive neuroplasticity addresses changes the nervous system’s ability to change in response to envi- that take place in response to biologically significant ronmental input and demands, is considered to be a key stimulus. Finally, many of the studies rely on animal postulate on which OT/SI is based. behavior; the links to human behavior are assumptions Implicit in Ayres’ early work is the idea that adequate and must be treated as such. sensory processing and integration is an important foundation for occupational role performance. Ayres hypothesized that some deficits in sensory processing and Findings integration will result in limitations in the production of Before beginning the literature review, search terms were adaptive behaviors and, as such, in participation. When defined and refined to focus results on studies emphasizing people experience deficits in sensory processing and in- sensory input as the independent variable and behavior or tegration, they struggle with the performance of everyday performance as an output. Details on the methodology occupations (Ayres, 1972; Bar-Shalita et al., 2008; Bundy underlying the search process are delineated in Arbesman & Murray, 2002; Gal et al., 2007). Adaptive responses, and Lieberman (2010). Search terms used included var- defined as successful interactions with the environment in iations of the following: neuronal or neural plasticity; response to environmental demand, can be seen as the neuroplasticity; neural receptors; nervous system ( building blocks for successful engagement and partici- and biochemistry, pathology); intersensory processes (includes pation in occupational roles. Thus, SI/sensory processing sensory integration); sense organs (physiology and bio- is of concern to occupational therapists. chemistry, pathology); sensory reception; sensation (physiology);

376 May/June 2010, Volume 64, Number 3 Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms neural coordination; psychomotor performance; perceptual reported in brain tissue weight, acetylcholine esterase motor processes; perceptual ; ; sensory (AChE) activity,1 total cholinesterase (ChE) levels, den- integration (keyword). As noted in the Arbesman and Lie- dritic branching, and number of synapses. berman (2010) article, searches were refined after review of Dendritic branching and increased number of syn- abstracts. Abstract review was based on relevance to the topic. apses are reflections of increased neuronal interactions Most articles included in this review were research based, and a sign of structural neuronal modification and in- although a few were reviews. Although the review emphasized creased complexity in neuronal interactions. Changes work accomplished in the past 15 yr; some older publications in dendritic branching in response to enriched envi- (e.g., Hubel & Wiesel, 1965) were included because they are ronments were reported by Diamond et al. (1972), considered key in the field of neuroplasticity. Fifty-nine Kempermann and Gage (1999), West and Greenough studies were identified to be of probable interest and rele- (1972), and Mollgarard, Diamond, Bennett, Rosenzweig, vance, and 50 were included in the final evidence table be- and Lindner (1971); all of these studies used cause they were deemed relevant to the question at hand. models. One classic example of environmental enrichment Table 1 is an abbreviated version of the original evidence can be found in the 1972 study conducted by Diamond table; the entire table can be viewed at www.ajot.ajotpress.net and colleagues. In this investigation, earlier findings doc- (navigate to this article, and click on “supplemental materi- umenting the effects of environmental enrichment and als”). Of the 50 studies included, 9 were Level I, 27 were Level impoverishment2 on the rat cerebral cortex were expanded II, 12 were Level III, and there was 1 study each at Levels IV to look specifically at the effects of age and duration of and V. The evidence table presented in this article includes exposure. Comparisons of cortical depth and cortical a sampling of all studies. The findings are summarized in the weight documented that the most drastic neuroplastic following sections by level (Levels I–IV), including key changes were evident in the EC rats at 25–55 days of age themes that might be extended to people with problems (roughly equivalent to 7–14 human yr) and that the processing and integrating sensory information. Finally, in findings were most pronounced in occipital and some- the Discussion section, we offer some interpretations and sthetic cortex. However, of great interest was the finding applications of this work to occupational therapists using that changes were also evident in the 60-to 90-day-old OT/SI. cohort (roughly equivalent to 16–24 yr in ), most robustly in the occipital cortex. Level I Studies In a second series of studies, in which data were in- cluded from animals exposed to the standard condition The Level I studies reviewed used a randomized controlled (see footnote 2) different effects between rearing con- trial design and span from 1969 to 2004. Most of this ditions depended on the age of animals and segments of research was done using rodents, comparing the effects of cortex studied. When comparing cortical depth to cortical enriched conditions (ECs) and deprived or impoverished weight, investigators found that active exploration was the conditions (ICs) on brain function. Because the studies critical component responsible for the changes in cortical used random assignment to experimental group, the de- depth (not visual stimulation alone). sign was strong. However, because most of studies were on These findings in rodents provide indirect support of animals, human application should be done with caution. at least one theoretical premise of OT/SI: Enriched en- Moreover, none of the studies specifically addressed OT/ vironmental conditions facilitate neural changes. Of in- SI, and as such the application of findings to clinical terest, the finding that active exploration is a necessary populations must be considered cautiously. This group of component of the brain changes described also lends studies supports the premise that environmental enrich- support for a central premise of OT/SI: that active en- ment alters brain structure and function in positive ways. gagement (of the child) is needed to facilitate SI. Finally, Changes after exposure to environmental enrichment are these investigations also indicated that objects should be varied and that the period of exposure required was at least 1 hr per day over a few weeks. This finding provides some 1Increases in both AChE and CHe levels reflects changes in acetylcholine activity (Giovannini et al., 2001; Gold, 2003). Some investigators use the ratio of AChE to ChE because it negates the effect of tissue weight on the 2EC offered opportunities for exploration, , play, and interaction with examination of activity changes. Acetylcholine is an excitatory neurotransmit- other animals. Play items were changed regularly. IC had small cages with solid ter associated with and neuroplasticity, For example, an side walls and no interaction with other animals. All animals had continual increase in acetylcholine release in the has been documented access to food and water. Standard condition was added in later studies to when animals experience novelty in the environment. This increase is con- evaluate the magnitude of the EC effects; wire cages were used so the animals current with improvements in cognitive performance. could see each other, and the cages were larger than those used for IC.

The American Journal of Occupational Therapy 377 Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms

378 Table 1. Neuroscience Evidence That Using a Sensory-Based Approach in Occupational Therapy With Children and Adolescents Is Effective

Intervention and Implications for Author/Year Study Objectives Level/Design/Participants Outcome Measures Results Study Limitations Occupational Therapy Braun et al. (2001) The objective was to Level III Intervention EMG activity greater during Although a functional task This study provides a means characterize the effects of Presentation of tactile writing than rest; expected (handwriting) was used, the to conceptualize short-term motor action on organization Design stimuli to first (D1, thumb) finding. situation in which it was neuroplastic changes that of somatosensory cortex in 1 group, nonrandomized and fifth (D5, little finger) tested was not contextually may occur during intervention. normal adults. digits of hand, right 3 2 EMG in the stimulated hand grounded. This may limit This study examined a Participants only increased during blocks, left 3 2 blocks, generalizability. Because highly trained motor task, 9 men and 3 women, ages writing condition where 24–43, all right handed within a session, random this study was done on handwriting, and suggests application within block to stimuli were applied to the typical adults, there may be that “task-dependent D1 or D5, each finger writing hand. limited generalizability to activation of preexisting receiving 500 stimuli. 2 MEG showed significant children or adults with maps might be a powerful sessions separated by 1 wk reduction of global field disability. mechanism to optimize of time. stimulus processing.” This activity of somatosensory- Task-specific activation of finding suggests that Behavioral measure during evoked field during writing. cortical connectivity development of such maps application of input: writing Motor activity exerts patterns may be reflective of for routine activities is without vision or rest. a gating influence on the how cortical networks important for optimal support optimal Outcome Measures processing of stimulus processing. Perhaps somatosensory input. performance.  Whole head MEG for improvements in routine task somatosensory-evoked The distance between D1 performance secondary to magnetic field and D5 representation grew practice relates to optimal measurement larger during writing, and stimulus processing.  Motor activity measured immediately became smaller from finger flexors and during rest. Data suggest extensors input to digits is processed  Electro-oculograms used separately during fine motor to control for eye tasks, minimizing cross-talk. movement artifacts Thus, functional organization Changes in functional of somatosensory cortex organization of somatosensory adapts dynamically to the requirements of a specific cortex were assessed by task. The task here was calculating the distance changes between highly trained (handwriting).

a/ue21,Vlm 4 ubr3 Number 64, Volume 2010, May/June representations of D1 and Findings were similar for left D5. and right hands.

Doucet et al. (2005) The objective was to Level II Intervention Blind participants fell into 2 Small sample size and This study provides examine the possibility that Stimuli were 30-ms noise groups on the basis of bias. a post priori group behavioral evidence of participants with blindness Design bursts ranging from Group membership was not assignment limit a difference in processing of are more efficient at 3 groups, cohort design 2–16 kHz broadband, linked to etiology of generalizability. sound in participants with processing spectral acoustic 2–3 kHz (low-pass), and blindness or presence of sight and some participants Participants The link to neuroplasticity is information to solve a task. Normally sighted humans 5–16 khz (high-band) residual vision. without sight. It suggests assumed, but there was no 5 presented at 40dBl SPL. that impairment of sensory (n 5) Findings were robust; measure of this.  Blind participants Sound was presented input changes the way the binaurally; monaurally to the previously shown with brain processes information; “without bias” (could psychophysiologic and PET accurately localize sound right ear (with left ear changes the skill with which obstructed with a soft foam techniques. Spectral information and is Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms

h mrcnJunlo cuainlTherapy Occupational of Journal American The both monaurally and plug and covered by haring alterations negatively processed. If this study is binaurally; n 5 5) protector muff); and affected blind participants’ generalizable to other  Blind participants “with binaurally with the contours ability to localize sound, sensory systems, it should bias” (localized sound of the ear pinna filled with suggesting they make better instill some contemplation of presented monaurally on acoustical paste (petroleum use of spectral information the impact of limited sensory the side of the open ear jelly) to equalize the circum- in the sound localization input on processing in other only; n 5 5) Groups were convolutions of the pinna. process. systems (i.e., avoidance of defined post priori on the touch). We may be able to basis of auditory testing. Outcome Measure Authors suggested that capitalize on enhanced skills Pointing with the dominant plasticity underlies the and better understand skill hand toward the perceived supranormal performance of differences. source of sound. participant with blindness.

Kempermann & Gage The objective was to Level I Intervention Sedentary mice were Animal study limits Authors introduced the (1999) examine experience- Enrichment involved 1 large heavier, but their generalizability. No blinding concept of novelty rather dependent in Design cage with toys, tunnels, and were not. for histology or behavioral than simply enrichment as the adult mouse At age of weaning (21 days), running wheels; periodic testing could bias results. being important in hippocampus as modulated rodents were randomized to extra treats (fruits and Enr group was less active hippocampal changes. Enr control, Enr, and Enr–WD when in activity chamber, by Enr and Enr–WD crackers) provided; appears to increase the 5 conditions (n 12/group). standard housing was 3/ indicating better habituation. potential for neurogenesis. cage with ad lib food and Subjects Rotarod performance was Authors suggest Enr water. Rodents better in Enr group and findings point to the need Exposure was 68 days, improved with practice. for continuous enrichment withdrawal for 28 days. No difference between with increasing complexity groups on swim maze, for best stimulation of Outcome Measures hippocampal neurogenesis.  although Enr group had Activity and habituation to They also suggest that new environment faster swim times. neurogenesis may have  Body and brain weight, Extension of previous work a ceiling. Thus, although motor coordination, (Enr resulted in increased findings are intriguing, if physical fitness, number of progenitor cells there is a ceiling effect of procedural learning on in hippocampus); longer neurogenesis, intervention rotarod exposure may preserve may find a limit.  Spatial learning using acute changes. WD tends to water maze testing, reverse changes, although immunohistochemistry, this was not significant in and immunofluorescence the current study. for cell count Enr increased new and cells not differentiated between neurons and astrocytes.

Rosenzweig & Bennett The objective was to define Level I Intervention Light is not essential to Animal study limits This study demonstrates (1972) environmental conditions Design EC exposure for 2 hr/day. obtain results from EC. In generalizability. Impossible that the rat brain has more 5 that bring about cerebral 6-group randomized study Intervention phase 30 the presence of light, rats to determine whether social plasticity than previously differences (EC vs. IC); with 6 experimental days showed results in the condition will have similar and that EC affects specifically, to determine conditions (IC = home cage; occipital cortex. findings in humans who are plasticity, but certain whether social grouping, or EC = enriched condition): social beings. conditions must be fulfilled 379 (Continued) Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms 380 Table 1. Neuroscience Evidence That Using a Sensory-Based Approach in Occupational Therapy With Children and Adolescents Is Effective (cont.)

Intervention and Implications for Author/Year Study Objectives Level/Design/Participants Outcome Measures Results Study Limitations Occupational Therapy whether social grouping, or 1. IC, saline injection Outcome Measures Brain weight in EC w/ to produce changes in brain exposure to EC during light 2. EC, saline injection, light Brain weight and chemical was weight and enzyme activity. or dark, were essential exposure analysis of brain tissue, greatest (facilitated This experiment also shows components 3. EC, saline injection, dark specifically ChE and ACHe movement and play during exposure activity. Calculated ACHe: EC in both dark and light) that active participation 4. IC, CHe ratio enhances plasticity. When 5. EC, light exposure, Social condition (EC with the rats were facilitated to other rats) showed play either by injection of methamphetamine injection moderate change; addition methylphenidate, prompting 6. EC, dark exposure, of methylhenidate resulted by the examiner, or other in more dramatic change, rats, the effects were methamphetamine injection presumably because rats greater. This finding Control: IC. were more active. supports a central premise of OT/SI: that active Methylphenidate only did Subjects participation is needed to not produce an effect. Rats optimally facilitate brain All 5 groups showed plasticity. significant difference from control group on ACHe:ChE ratio (a sensitive measure of effects that cancels out variable of brain weight).

Rosenzweig et al. (1969) The objective was to study Level I Intervention EC: Significantly greater Animal study limits EC produced measurable the exact nature and extent Design EC included brightly lit cortical tissue weight, total generalizability. Study brain differences in adults of the cerebral difference Random assignment with 3 rooms, housing in groups, AChE activity, total ChE, and measures brain without and young, which suggests that develops between conditions: ECT, EC, and IC. and providing toys. ECT was cortical depth. Results providing concurrent that visual input alone is not enriched experience and the same as EC with daily occurred as clearly in adults measures of behavior; responsible for these impoverished experience EC: brightly lit rooms, exposure (30 min) to open as in young rats. therefore, it is not possible changes but that the sensory rats in the occipital cortex. housed in groups, provided field environment in which to relate brain changes to systems work together to toys, etc. patterns of barriers was ECT vs. IC (tissue weights, behavioral changes. produce changes. This study changed. cortical size): significant provided support for the idea a/ue21,Vlm 4 ubr3 Number 64, Volume 2010, May/June ECT: same as EC with differences; greatest Visual experience is not that sensory input can shape exposure daily (30 min) to Outcome Measures difference in occipital a necessary component of brain activity. open field environment in Dissection, weighing, and cortex, least difference in the conditions that evoke which pattern of barriers chemical analysis of brain somesthetic cortex. change. was changed Change in AChE and ChE Included blind analysis of activity greatest in the results. occipital area. Subjects ChE:AChE ratio (measure of Rats glial cell) was greatest in occipital region, although this was present in all regions. Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms

h mrcnJunlo cuainlTherapy Occupational of Journal American The Cortical depths greatest in occipital area in EC rats.

Stoeckel, Pollok, Schnitzler, The objective was to study Level I Intervention Study 1: Participants using Small experimental group fMRI evidence for cerebral Witte, & Seitz (2004) use-dependent plasticity of None their feet for everyday size (F2 N 5 3) limits reorganization is consistent human somatosensory Design activities had significantly generalizability. with behavioral data. Use cortex. 3 groups, randomized: Outcome Measures fewer errors (6%) on the dependent is defined as  Used feet for certain Study 1: Accuracy of tactile localization test than everyday activities—this is Study 1: Determined actions only (n 5 10). localization of tactile stimuli the comparison group (P 5 important for occupational  differences in accuracy of Used feet extensively for on toes; examined cortical .003, 1-tailed). therapy. Use-dependent localization of tactile stimuli everyday activities such representation between plasticity appears to depend on toes between partici- as writing and eating groups (fMRI): Study 2: Activation in S1 of on at least 2 principles: 5  pants who (1) used feet to (n 3). Threshold for detection of somatosensory cortex was 1. Representation of areas  accomplish simple tasks Control group; tactile stimuli on each toe significantly stronger in of body parts used with (the F1 group); (2) used thalidomide-damaged determined. participants who used feet high frequency tend to toes to accomplish everyday extremities but normal  Threshold monofilament for everyday activities (ps 5 expand, and activities such as writing hands; feet not used for was chosen to evaluate .002–137). 2. Simultaneous stimulation and eating (the F2 group); any unusual actions localization for all toes. of body parts leads to and (3) control participants. (n 5 10). Study 2: fMRI activation of integrated, overlapping Study 2: Determined Participants somatosensory area during representational cortical differences in somato- People with thalidomine- tactile stimuli fields. sensory activation patterns affected upper extremity Both principles are inherent 5 to tactile stimuli on toes (n 23). in the OT/SI approach. between the 3 groups. 5 5 Mean age 39.8 (range In addition, study provides 39–42). support for OT/SI theory and practice with supporting evidence that “everyday activities” enhance neural (and behavioral) organization.

Wiesel & Hubel (1974) The objective was to Level II Intervention Highly ordered sequences of Animal study limits The theory of OT/SI is built determine whether ordered n 5 4 monkeys with eyes orientation shifts were generalizability. on idea that early sensory sequences of orientation Design 2 groups, sutured shut at various present and were not experiences shape brain nonrandomized columns are present in very times close to time of birth; different from what is seen development and influence young, visually naı¨ve Subjects 2 control participants in adults, suggesting that learning and behavior. This monkeys. Macaque monkeys (n 5 6) the organization of the study supports this Outcome Measures columns of the foundational concept Recordings from Area 17 is innately determined and showing that although the (occipital cortex) NOT the result of early visual system is innately experience. In addition, there organized, lack of was deterioration of innate experience (i.e., no vision) connections subserving results in diminished binocular convergence connections. suggesting that deprivation This study addresses the results in deteriorating effects. nature–nurture issue and shows that although the 381 (Continued) Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms 382 Table 1. Neuroscience Evidence That Using a Sensory-Based Approach in Occupational Therapy With Children and Adolescents Is Effective (cont.)

Intervention and Implications for Author/Year Study Objectives Level/Design/Participants Outcome Measures Results Study Limitations Occupational Therapy visual system is guided by genetic factors, postnatal environmental influences are needed for optimal development.

You et al.(2005) The objective was to Level V Intervention Bruininks–Oseretsky Test of Single-subject design limits These virtual reality activities determine whether virtual Single-subject study with Motor Proficiency score generalizability. targeted specific functional reality therapy would Design pretesting and posttesting changed from 1 to 5. aspects of movement. Using Case report Use of isolated items from promote practice-dependent actual body movement and plasticity in a child with CP, Intervention conducted by Pediatric Motor Activity Log standardized assessment virtual reality feedback for Participant a therapist unaware of the increased amount of use tools without substantiation leading to enhanced motor 8-yr-old boy with knowledge of results (visual skills and overcoming research and quality of movement. of their ability to stand and proprioceptive feedback) hemiparetic CP on right side alone; intensity of nonuse. in a manner that was Virtual reality games that Fugl–Meyer assessment intervention precludes its included -ball, conveyor, score increased from 39 to perceived as playful and reimbursement potential. gamelike, this study indicates and soccer. 52, showing enhanced However, the study active movement control, that a controlled sensory Intervention was 60 min/ suggests that using actual environment can result in a reflect activity, and body movement and virtual day, 5 days/wk, for 4 wk. coordination in upper combination of functional reality feedback for changes and neuroplasticitic Outcome Measures extremity. knowledge of results (visual  changes in critical cortical fMRI fMRI showed a change in and proprioceptive feedback)  regions. Bruininks–Oseretsky Test activation pattern. in a manner that was of Motor Proficiency, item Preintervention activation perceived as playful and 6: touching a swinging involved bilateral primary gamelike, (controlled sensory ball motor and sensory cortices, environment) can result in  Modified Pediatric Motor sensorimotor cortex, and a combination of functional Activity Log ipsilateral supplemental changes and neuroplasticitic  Upper limb subtest of motor areas. changes in critical cortical Fugl–Meyer assessment. regions. No activation of premotor cortex postintervention showed loss of aberrant a/ue21,Vlm 4 ubr3 Number 64, Volume 2010, May/June activation and primary activation of the sensorimotor cortex and contralateral primary sensory and motor cortices.

Note. AChE 5 acetylcholinesterase; ChE 5 cholinesterase; CP 5 cerebral palsy; EC 5 enriched condition; ECT 5 enriched condition with training; EMG 5 electromyography; Enr 5 long-term stimulation (enrichment); Enr–WD 5 long-term stimulation and withdrawal; fMRI 5 functional magnetic resononance imaging; IC 5 impoverished condition; MEG 5 magnetoencephalography; PET 5 positron emission tomography. basic science data that may inform investigations related to 38%. Moreover, the physical performance improvements the optimal length and frequency of intervention (also were associated with an increase in activation of contra- known as dosage). No behavioral measures were included lateral primary motor and sensory areas and the striatum in this first series of studies; no direct inference between along with decreased cerebellar activation. Different areas brain changes and behavior changes can be made. of activation change were seen in the mental practice group, West and Greenough (1972) worked to link neuro- suggesting different mechanisms of plasticity. The motor nal changes to behavioral improvements. They exposed improvement in the physical performance group suggests animals to similar complex environments and found that that active participation, which provides somatosensory the length and thickening of the synaptic boutons were feedback, is important in motor improvement. This find- greater in the EC rats compared with the IC rats (see ing is consistent with SI theory constructs. footnote 2). Rats exposed to EC were also better at per- Additional support for the finding that active ex- forming a maze task, suggesting that changes in neuronal ploration, not merely seeing the stimuli, is a critical in- structure are related to behavioral improvements. gredient in neural changes was documented by other Kempermann and Gage (1999) also supported the investigators. Examining the impact of enrichment premise that ECs can alter brain activity and structure. compared with simple visual exposure, Rosenzweig and They studied whether experience-dependent neurogenesis colleagues (1969) found that neuroplastic changes in the in the adult mouse hippocampus is modulated by long- occipital cortex do not require light exposure; conversely, term stimulation; they compared this condition to long- active exploration of the environment was crucial. In term simulation and withdrawal. Enrichment (one large other words, the animals needed to do the exploration cage with toys, tunnels, and running wheels and periodic themselves; simply being exposed to the environment extra food treats) increased the number of new neurons without exploring it was not sufficient to result in neu- and cells. However, there was not increased differentia- roplastic changes. In subsequent examination of what tion between neurons and astrocytes, leading investigators might be influencing the changes, investigators compared to conclude that enrichment may increase the potential rats with increased activity level with rats that were for neurogenesis. Withdrawal of the enriched environ- prompted into activity by the experimenter. They found ment tended to reverse the changes noted, but this re- that the rats not needing to be prompted into activity in versal did not reach significance. This study adds to the ECs had the most profound cortical changes, al- Kempermann and Gage’s previous work by showing that though the extent of the effect varied depending on the longer exposure may preserve acute changes. This work cortical area measured (Rosenzweig & Bennett, 1972). also builds on the classic studies of Diamond and col- This investigation also examined AChE and ChE activity, leagues (1992), providing evidence that (1) exposure to finding changes parallel to those for cortical depth. In- enriched environments increases cell number, neurogenesis, vestigators drew several interesting conclusions from this or the potential for neurogenesis and (2) there may be and previous studies. First, placing rats in a large but a need for continuous enrichment with increasing com- empty cage had no effect on cortical depth or AChE plexity for best stimulation of hippocampal neurogenesis. activity. However, a complex environment coupled with A more contemporary study of brain–behavior rela- enhanced activity resulted in profound neuroplastic tionships in humans was conducted by Lacourse, Turner, changes in the brain, both in terms of cortical structure Randolph-Orr, Schandler, and Cohen (2004). These and enzyme activity. Moreover, effects were greatest if authors compared physical performance of a learned task exposure to EC took place during the rat’s most active (pushing a button in a sequence with different fingers) period of its circadian cycle. Thus, findings indicated that with mental practice and no practice, using blood- active participation or exploration was crucial; changes oxygen-level–dependent functional magnetic resonance were most profound when animals were internally driven imaging. Investigators examined areas of cortex and cer- (rather than externally prodded) to increased interaction ebellum activated and performance level. Physical perfor- with the environment. This finding lends support to mance participants practiced a sequence of button presses a central premise of the OT/SI frame of reference: that for 1 wk; mental practice participants practiced through active participation by the child is needed to optimally motor imagery; no-practice participants did not practice. facilitate brain plasticity. Investigators found that the physical performance group Level I studies offer the most rigorous study design, demonstrated the most improvements in behavior (121% making the findings here of great interest. The fact that all improvement); the mental practice group demonstrated but one of the studies reflected here, and all but two 86% improvement; and the no-practice group improved reviewed for this project, were conducted on animals

The American Journal of Occupational Therapy 383 Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms makes the application to the human population somewhat & Tesche, 2005; Recanzone, Schreiner, & Merzenich, tenuous. This fact can be countered by noting that there is 1993). The mechanisms for these changes included in- consistency across animal models (e.g., rat, mouse, gerbil, creased dendritic branching (Volkmar & Greenough, cat), suggesting that the findings are not specific. In 1972), histological changes (in cell structure and func- broad terms, what these Level I studies point to is the tion; Volkmar & Greenough, 1972), anatomical changes importance of active exploration of complex environments (in sensory and motor maps or reorganization of brain for neuroplastic changes to occur in the brain; it appears to areas), changes in cellular activation patterns (Bennett be important that engagement be ongoing rather than et al., 1964; Recanzone et al., 1993), and, most recently, a single experience. Moreover, doing (physical perfor- through upregulation of (increasing expres- mance) has a different effect than thinking about doing. sion) associated with neuroplasticity by means of brain- Each of these ideas can be extrapolated, cautiously, to derived neurotrophic factor (BDNF; Go´mez-Pinilla, Ying, some of the tenets of SI theory. The sensory nature of these Roy, Molteni, & Edgerton, 2002).3 studies was generally broad; animals in EC conditions As was the case for Level I studies, results from Level II explored their environments, getting input through all animal studies are shown most consistently in response to sensory channels. In the Lacourse et al. (2004) study, ECs (opportunities for sensory, motor activity, and social human participants similarly obtained a broad range of interaction; Bennett, Rosenzweig, Diamond, Morimoto, sensory input from engagement in practice. This too is & Hebert, 1974; Brown et al., 2003; Kempermann, consistent with the theory of SI, as proposed by Ayres Kuhn, & Gage, 1998) and in the visual and auditory (1972). Although Ayres’ original work emphasized tac- systems (Moses et al., 2005; Recanzone et al., 1993). tile, proprioceptive, and vestibular inputs, OT/SI capi- Neuroplastic changes are also documented in the so- talizes on enhanced sensory opportunities in all sensory matosensory cortex but less consistently (Merzenich, systems, consistent with that seen in these studies. Recanzone, Jenkins, & Grajski, 1990; Wu, van Gelderen, Hanakawa, Yaseen, & Cohen, 2005). The documented changes may not be global (i.e., in the entire nervous Level II Studies system) but rather specific to precise areas of the central Level II studies are those that compare at least two groups nervous system—the hippocampus being one of these but in which randomization of subject to group has not areas (Kempermann et al., 1998). been used. Examples of Level II studies include cohort and These same concepts are supported in the human case–control designs. Of the Level II studies reviewed, 9 studies, but the data are not as strong because of limi- used human participants, 2 used nonhuman primate tations in studying tissue and processing participants, and 16 used other animals (primarily rodent (Bach-y-Rita, 2004; Mercado et al., 2001). The human models, with some mammal models). The studies re- studies do, however, demonstrate that (1) the auditory viewed spanned from 1964 to 2005 and provide evidence system demonstrates plasticity both in its processing that supports neuroplasticity in the central nervous sys- (activation patterns) and cortical representation in re- tem in response to sensory input. A variety of models sponse to auditory input (Bangert & Altenmu¨ller, 2003; and designs was used, including exposing animals to Doucet et al., 2005; Moses et al., 2005); (2) the brain ECs, the results of altered or enhanced sensory input processes stimuli differently because of either training (e.g., training to enhance auditory or tactile discrimi- (piano playing) or ECs (Ro¨eder, Ro¨sler, & Neville, nation skills; Bangert & Altenmu¨ller, 2003; Mercado, 2000); and (3) processing of sensory stimuli is dynamic Bao, Ordun˜a, Gluck, & Merzenich, 2001; Zhang, Bao, and flexible; that is, the sensory systems used during & Merzenich, 2001), and the effects of sensory alterations a task are flexible and dependent on the task presented (caused by congenital or induced lesions such as blindness (Russo, Nicol, Zecker, Hayes, & Kraus, 2005). Addi- and deafness) on brain processing and functions (Doucet tional human studies (Doucet et al., 2005; Sober & et al., 2005; Hubel & Wiesel, 1965; Stryker & Sherk, Sabes, 2005) demonstrated plasticity in human sensory 1975). systems. For example, participants who have blindness For the sake of brevity, the animal data are broadly demonstrate auditory system reorganization such that summarized here. In numerous studies, strong support they become more efficient at processing auditory cues that sensory input (altered or enhanced) changes the way the nervous system processes information was provided 3BDNF is a brain protein and neurotrophic factor. It can promote increased (Bennett,Diamond,Krech,&Rosenzweig,1964;Gordon neuronal survival as well as the growth of new neurons, and it has been found & Stryker, 1996; Moses, Martin, Houck, Ilmoniemi, in areas linked to learning and .

384 May/June 2010, Volume 64, Number 3 Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms (Doucet et al., 2005). Sober and Sabes (2005) demon- a task resulted in changes in tactile discrimination ability. strated that the use of sensory cues was dynamic, flexible, For instance, using magnetoencephalography (MEG)4 as and dependent on availability; participants could readily an outcome measure, Schaefer et al. (2005) found more shift their degree of reliance on vision or propriocep- distant and distinct somatosensory cortical finger repre- tion, depending on what was available during a reaching sentation when Digits 1 and 5 were stimulated during task. a fine motor/cognitive task than when participants were Level II studies reinforced outcomes related to EC “at rest.” The plasticity was highly task dependent and identified in Level I studies and provided some interesting dynamic in that changes were shown during task perfor- information about human sensory processing. They mance. These investigators concluded that changes to the suggested that deficits in one sensory modality result in somatosensory cortex are dynamic and task specific. alterations in how the brain processes information in other Moreover, the fact that changes were greater during tasks modalities and that a typical nervous system can flexibly that required cognitive processing suggested that dynamic rely on the sensory information available within the en- plasticity can be facilitated by activation of frontal and vironment to complete a task. This last point offers some . support for the SI theory assumption that a successful The integration of visual and auditory sensory input environmental interaction promotes processing and in- was investigated by Moses and colleagues (2005), also tegration of sensory information. In this case, success using MEG. These investigators presented paired visual depended on the participant’s ability to blend visual and and auditory stimuli and noted activation in expected proprioceptive strategies. Both studies used adults as brain regions. Subsequently, presentation of a visual participants; mature nervous systems may process in- stimulus alone resulted in specific MEG responses in the formation differently from developing nervous systems. . These investigators interpreted this finding as “associative neural plasticity” (p. 787). The demonstration in this study that the presentation of Levels III, IV, and V sensory information from one modality can produce Studies at Levels III, IV, and V are characterized as single- brain activity in the primary cortex of another sensory group, nonrandomized (III); single-subject design, case modality suggested that the processing of sensation from series (IV); or case reports/expert opinion (V). Those different modalities is linked when the sensations are reviewed here spanned 1967 to 2005 and included many paired. Because our world is not one of single-channel human studies, as well as studies on monkeys, kittens, and sensory inputs, pairing of sensation is the rule, not the rats. Early studies of in animal models dem- exception. This rule is a foundation of OT/SI; sensations onstrated that the sensory systems had an innate and pre- are intended to be meaningfully paired such that input determined organization but that this organization was in one sensory modality can be used to influence dependent on sensory input and experience for full ex- processing in another modality. Because the Moses et al. pression of function (Wiesel & Hubel, 1965, 1974). Le- (2005) study was specific to the auditory and visual sys- sions resulted in reactive morphological and physiological tems, application to other sensory systems must be done changes in sensory systems, suggesting that the brain re- cautiously. organizes when deprived of specific sensory input. This Also of interest in these studies was the degree of finding was supported behaviorally in the Doucet et al. coding engaged in by the brain. Coding refers to the (2005) study described previously. Studies such as that of process of programming activity in brain regions needed Hubel and Wiesel (1965) also showed that there were to produce the desired response. Less coding is needed for critical periods for development and restoration of function simple tasks, and the brain appears to allocate only the after lesion and that function did not necessarily return resources needed for the task. Examining coding of tex- after a period of deprivation or lesion. Thus, there appear ture within the tactile and visual systems, Guest and to be limits to degree of plasticity in organization and Spence (2003) demonstrated that participants used both function. vision and touch in accomplishment of a task only if the Reactive neuroplasticity, documented behaviorally by task specifically required it. Integration of both sensory Sober and Sabes (2005) and described earlier, was iden- modalities did not take place when tasks were very tified in the organization of human somatosensory cortex (Schaefer, Heinze, & Rotte, 2005; Wu et al., 2005). This

region of the brain was shown to adapt dynamically to 4MEG is a highly sensitive imaging technique measuring the magnetic fields requirements of a specific task; sensory input during produced by the brain’s electrical activity.

The American Journal of Occupational Therapy 385 Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms simple, suggesting that multi-SI may depend on task using multiple intervention frames of reference, work to difficulty or complexity. facilitate successful participation in life activities. More Halder et al. (2005) examined movement repetition specific to OT/SI, successful participation in life activities and practice in 10 healthy adults, using a nonskilled task is supported through the provision of an enriched environ- (power grip using vision to control force). Electroenceph- ment. Using OT/SI, the “enriched environment” is designed alogram measurements indicated different changes to match expectation for performance with the client’s skills in neural activity at each stage of the motor task (prepara- and offer the “just-right challenge” to promote processing and tion, movement execution, and feedback integration). The integration of sensory information. In this respect, OT/SI researchers concluded that, in a motor task, distinct differs from the foundational work on neuroplasticity, in mechanisms of plasticity occur during specific stages of that the enrichment is specific to the individual’s needs and information processing and, with practice, motor vari- thus neuroplastic changes may be individually driven; ability decreases. This finding suggests a role for sensory however, this application warrants investigation. feedback mechanisms in various stages of motor task exe- Building on these classic studies, investigations of cution, an example of sensory–motor integration. More- specific sensory interventions reported on in this review over, using single-case design, You et al. (2005) noted that documented changes in central nervous system function, training, either actual or using virtual reality, resulted in organization, and structure after sensory manipulations. A reorganization of cortical regions that were associated with few key points are particularly relevant to OT/SI: changes in performance, again suggesting a role for feed- • The sensory environment and environmental oppor- back, either actual sensory feedback or virtual feedback. tunities or affordances generally affect brain structure Together, the findings here suggest that neuro- and function (e.g., Bennett et al., 1974; Diamond plasticity is dynamic and that the sensory systems interact et al., 1972; Kempermann & Gage, 1999; West & such that pairing influences processing. Sensory strategies Greenough, 1972). used are typically task and experience specific, and sensory • Noted changes are often, although not invariably, processing strategies can be linked to stage of motor documented in behavior and in brain structure and performance. Globally, these findings support the tenets of function (e.g., Halder et al., 2005; Russo et al., SI theory as proposed by Ayres (1972). 2005; You et al., 2005). • All regions of the brain do not show the same response to either specific sensory activation or enriched envi- Discussion ronments (e.g., Mercado et al., 2001). This review provides direct and robust support for neu- • Changes can be task specific, making it important to roplasticity in many brain regions in response to ECs or be focused in terms of outcome measures (e.g., Halder direct sensory input, which can be enhanced during motor et al., 2005; Recanzone et al., 1993). activity. Findings indicated that changes in neuronal • Changes are highly dynamic and seen very quickly function and structure, and in some studies changes in (e.g., Pantev et al., 2003). behavioral indexes, were linked to these neural mod- • Changes can be long lasting, depending on the person ifications. Many of the investigations reviewed here were and the environment (e.g., Stoeckel et al., 2004). conducted on animals; those on humans typically used • Some sensory systems have “critical periods” when adults; both of these facts limit the application of the processing changes may be easier to document or findings to OT/SI. times when processing centers are more readily influ- Nonetheless, many interesting parallels can be drawn enced by sensory input (e.g., Bavelier et al., 2001; between these basic science studies and Ayres’ (1972) SI Zhang et al., 2001). theory. First, several of the studies reviewed described • Documentation supporting interaction among sensory experimental manipulations that paralleled individual SI systems exists; stimulus pairing may be an effective theory premises. First, the classic studies of environ- intervention tool. However, it is used as needed; if mental enrichment (e.g., Bennett et al., 1974, 1996; the task is simple, only one sensory modality may be Diamond et al., 1972; Rosenzweig & Bennett 1972; needed, and integration of modalities does not occur Rosenzweig et al., 1969) provided early evidence that (e.g., Guest & Spence, 2003; Hodzic, Veit, Karim, neuroplasticity is possible and that the environment has Erb, & Godde, 2004; Moses et al., 2005; Sober & an impact on neural structure and function. This finding Sabes, 2005). has tremendous implications for occupational therapy in • It is important to consider the cognitive demands as- general and OT/SI specifically. Occupational therapists, sociated with a given task because these appear to have

386 May/June 2010, Volume 64, Number 3 Downloaded From: http://ajot.aota.org/ on 01/26/2015 Terms of Use: http://AOTA.org/terms an effect on motor output and sensory processing to a specific task. This idea is supported in the human (e.g., Braun et al., 2001; Kourtzi, Betts, Sarkheil, & data demonstrating that brain processing of sensory input Welchman, 2005). is flexible and dynamic and that the greatest changes • Rich sensory input, contextualized in meaningful activ- come when interaction with the environment is not ity, facilitates neuroplasticity and thus growth, develop- forced but rather self-initiated (vanPraag, Kempermann, ment, and behavior (e.g., Go´mez-Pinilla et al., 2002). & Gage, 1999). There is little question that the nervous system is Another principle of the SI frame of reference that is plastic and that sensory input is an important mediator of supported is the notion that enriched sensorimotor ex- this plasticity. Motor activity and interest in task also perience enhances the brain’s processing of information appear to be important contributors, and active en- and provides a foundation for learning. This principle is gagement is seen to enhance the effects. Moreover, these demonstrated in studies showing that ECs (sensory, studies indicated that neuroplastic changes were de- motor, and problem-solving opportunities) produce velopmental, dynamic (reactive), and task specific. In this neuroplastic changes in areas of the brain related to regard, these data provide indirect support for the use of learning and memory—for instance, the hippocampus— OT/SI, which is built on the premise that active en- that were concurrent with behavioral improvements in gagement in meaningful, sensorimotor activities at the learning (Kempermann & Gage, 1999), thus supporting just-right challenge and in a playful or meaningful context Ayres’ (1972) original notion that sensorimotor activity has a positive impact (by means of neuroplasticity) on provides a foundation for learning. processing in the nervous system (Ayres, 1972). Beyond this support, the studies reviewed inform us that multi-SI Authors’ Note may be task specific or dependent on task complexity. This review of neuroplasticity literature is necessarily This finding warrants consideration in the provision of limited. The entire body of this literature is vast, OT/SI. expanding across many decades and professional areas. Applied to OT/SI, the message is that tasks intended This project was initiated in 2005; as such, the review to tap into more than a single sensory processing system includes materials felt to reflect the literature up to that must do so naturally if integration is to be seen. For in- date. Since the conclusion of this review, additional re- stance, if we are hoping to integrate proprioceptive and search has been published that continues to add support to visual inputs, then swinging on a trapeze over a bolster and the conclusions reached in this investigation. Reflecting on targeting a pile of pillows as the drop point has the po- these publications goes beyond the intent of this article. tential to be integrative; this activity combines pro- This is an area of growing interest, likely to continue to prioceptive (muscle contraction involved in hanging on scaffold support for the effectiveness of sensorimotor– and flexing the trunk to clear the bolster), vestibular based interventions on improving task and role perfor- (swinging and linear movement), and visual (identification mance. It is time occupational therapists joined this of the target) inputs in a natural and highly motivating movement fully, adding their collective voices to this manner. Conversely, passive input (e.g., passive spinning, body of neuroscience knowledge and providing the sci- passively applied touch) would appear not to create the entific evidence needed to better understand the effec- same affordance for integration. tiveness of OT/SI. s In looking to address the specific question posed for our investigation (i.e., What is the neuroscience evi- References dence that using a sensory-based approach in occupational therapy with children and adolescents will be effective?), Ahn, R. R., Miller, L. J., Milberger, S., & McIntosh, D. N. (2004). Prevalence of parents’ of sensory pro- the studies examining environmental enrichment provide cessing disorders among kindergarten children. American the closest match to OT/SI because they offer the par- Journal of Occupational Therapy, 58, 287–293. ticipant (animal or human) control over activity, novelty, Arbesman, M., & Lieberman, D. (2010). 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