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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, brain
 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, 375390. doi: 10.5014/ajot.2010.09069

Shelly J. Lane, PhD, OTR/L, FAOTA, is Professor and


Chair, Department of Occupational Therapy, Assistant
Dean for Research, School of Allied Health Professions,
W hat is the neuroscience evidence that occupational therapy using a sensory
integrative framework with children and adolescents will be effective? This
question was designed to investigate the basic neural and developmental science
Virginia Commonwealth University, 730 East Broad Street,
Suite 2050, Richmond, VA 23219; sjlane@vcu.edu 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 nervous system to process sensory information, enhance the orga-
nization and integration of sensation, and, as a result, have a positive impact on
the childs ability to participate in daily life activities (Ayres, 1972, 1979).

The American Journal of Occupational Therapy 375


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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 brainbehavior 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 environmental enrichment 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. human 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., rodents
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, Alternmuller, &
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
topic we examined in this review, neuroplasticity, defined as development and reactive neuroplasticity addresses changes
the nervous systems 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 (physiology
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


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neural coordination; psychomotor performance; perceptual reported in brain tissue weight, acetylcholine esterase
motor processes; perceptual motor learning; perception; 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 rodent
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 IIV), including key changes were evident in the EC rats at 2555 days of age
themes that might be extended to people with problems (roughly equivalent to 714 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 1624 yr in humans), most
robustly in the occipital cortex.
In a second series of studies, in which data were in-
Level I Studies
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
1
Increases in both AChE and CHe levels reflects changes in acetylcholine
activity (Giovannini et al., 2001; Gold, 2003). Some investigators use the
2
ratio of AChE to ChE because it negates the effect of tissue weight on the EC offered opportunities for exploration, exercise, 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 neuromodulation and neuroplasticity, For example, an side walls and no interaction with other animals. All animals had continual
increase in acetylcholine release in the hippocampus 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


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

378
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
9 men and 3 women, ages blocks, left 3 2 blocks, generalizability. Because highly trained motor task,
within a session, random writing condition where this study was done on handwriting, and suggests
2443, all right handed stimuli were applied to the
application within block to 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. activity of somatosensory- stimulus processing. This
Task-specific activation of
evoked field during writing. finding suggests that
Behavioral measure during 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
processing of support optimal
Outcome Measures stimulus processing. Perhaps
somatosensory input. performance. improvements in routine task
 Whole head MEG for
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

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 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).
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 216 kHz broadband, linked to etiology of generalizability. sound in participants with
processing spectral acoustic Participants 23 kHz (low-pass), and blindness or presence of sight and some participants
information to solve a task. 516 khz (high-band) residual vision. The link to neuroplasticity is without sight. It suggests
Normally sighted humans
presented at 40dBl SPL. assumed, but there was no that impairment of sensory
(n 5 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

May/June 2010, Volume 64, Number 3


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 brains generalizability. No blinding concept of novelty rather
dependent neurogenesis in Design cage with toys, tunnels, and were not. for histology or behavioral than simply enrichment as
At age of weaning (21 days),

The American Journal of Occupational Therapy


the adult mouse 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 EnrWD when in activity chamber,
by Enr and EnrWD crackers) provided; appears to increase the
conditions (n 5 12/group). standard housing was 3/ indicating better habituation. potential for neurogenesis.
Subjects cage with ad lib food and Rotarod performance was Authors suggest Enr
Rodents water. 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

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 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 neurons
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
that bring about cerebral 6-group randomized study Intervention phase 5 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 thought 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

(Continued)

379
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 methylphenidate 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, methamphetamine 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 participation is needed to
Subjects
not produce an effect. optimally facilitate brain
Rats
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).

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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
ECT: same as EC with differences; greatest Visual experience is not
exposure daily (30 min) to Outcome Measures that sensory input can shape
difference in occipital a necessary component of
open field environment in Dissection, weighing, and brain activity.
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.

May/June 2010, Volume 64, Number 3


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 activitiesthis 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:
pants who (1) used feet to (n 5 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

The American Journal of Occupational Therapy


activities such as writing hands; feet not used for was chosen to evaluate .002137). 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). integrated, overlapping
Study 2: fMRI activation of
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
to tactile stimuli on toes (n 5 23). in the OT/SI approach.
between the 3 groups.
Mean age 5 39.8 (range 5 In addition, study provides
3942). support for OT/SI theory
and practice with supporting
evidence that everyday

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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 nave 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 visual system 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. naturenurture issue and
shows that although the

381
(Continued)
Table 1. Neuroscience Evidence That Using a Sensory-Based Approach in Occupational Therapy With Children and Adolescents Is Effective (cont.)

382
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 BruininksOseretsky 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. Virtual reality games that FuglMeyer assessment in a manner that was
intervention precludes its perceived as playful and
included bird-ball, conveyor, score increased from 39 to
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
 fMRI changes in critical cortical
fMRI showed a change in and proprioceptive feedback) regions.
 BruininksOseretsky Test activation pattern. in a manner that was
of Motor Proficiency, item perceived as playful and
Preintervention activation

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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 changes and neuroplasticitic
ipsilateral supplemental
 Upper limb subtest of motor areas. changes in critical cortical
FuglMeyer assessment. regions.
No activation of premotor
cortex postintervention
showed loss of aberrant
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); EnrWD 5
long-term stimulation and withdrawal; fMRI 5 functional magnetic resononance imaging; IC 5 impoverished condition; MEG 5 magnetoencephalography; PET 5 positron emission tomography.

May/June 2010, Volume 64, Number 3


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 Gages 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 brainbehavior 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 rats 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-leveldependent 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

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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 species 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 genes (increasing gene 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; Gomez-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 systemthe 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
casecontrol 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 human brain 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 & Altenmuller, 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 (Roeder, Rosler, & Neville,
nation skills; Bangert & Altenmuller, 2003; Mercado, 2000); and (3) processing of sensory stimuli is dynamic
Bao, Orduna, 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 3
BDNF 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 memory.

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(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 prefrontal cortex.
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 participants 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. auditory cortex. 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 visual cortex 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 4
MEG is a highly sensitive imaging technique measuring the magnetic fields
requirements of a specific task; sensory input during produced by the brains electrical activity.

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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 clients 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 individuals 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 sensorymotor 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

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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., Gomez-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 brains 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 memoryfor 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-
dence that using a sensory-based approach in occupational
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