Sensory Modulation: A Review of the Literature Authors: Julia

Sensory Modulation: A Review of the Literature
Authors: Julia Wilbarger, MS, OTR and Tracy Murnan Stackhouse, OTR
The concept of a disruption in sensory modulation (SMD) has emerged recently as a "hot-topic" within the field of
occupational therapy. This was evident at the recent AOTA Annual Conference in Baltimore (April, 1998), where
the Sensory Integration Special Interest Section, currently chaired by Jane Koomar, devoted a full day to an
institute on sensory modulation. Several OT researchers, some of whom presented at the AOTA Institute, have
published or are in the process of publishing new studies related to disruption in sensory modulation in a variety
of clinical and normative samples. Additionally, there were several short course and paper topics focusing on this
area of theory and practice.
Due to the increasing interest in sensory modulation, it is increasingly important for OT practitioners,
researchers, and educators to have a common way to discuss and disseminate information relevant to the area.
However, there is limited information written about sensory modulation. Further, referring to this cluster of
problems as a disorder may be premature. Our understanding of the nature of this phenomenon is in the very
early stages. It has not been identified as having universal and persistent features that are distinct from other
established disorders. To that end, it may be more appropriate at this time to describe SMD as a disruption in
processing rather than trying to define it as a disorder. (Note: We will use the term disruption but will refer to
disorder in our historical review to maintain the authors’ terminology)
Within the field of occupational therapy, current theorists rely upon the core writings of Dr. A. Jean Ayres. Her
theory of sensory integration provides the inceptive principles upon which later theorists have built. However,
Ayres’ descriptions of the modulation of sensory input are only the beginning. Over the last three decades, the
concept of sensory modulation has been informed by the clinical practice of occupational therapists using a
sensory integrative frame of reference. This field has expanded the application of occupational therapy
intervention to a variety of clinical populations -- each providing insight into sensory processing phenomenon
and how disruptions of sensory processing can lead to a variety of problems with carrying out "the skills for the
job of living".
The concepts supporting sensory modulation also have evolved in accordance with new findings from
neuroscience. As 1990 was deemed the "Decade of the Brain," many changes in thinking have occurred over
the course of the last 30 years that need to be incorporated into any theory of brain-behavior relationships. Most
prominently, the notion of a hierarchically organized brain has been replaced by a heterarchical, parallel,
distributed processing model of brain structure and function. Theoretical models derived from less complex brain
system representations do not offer a current conceptualization of what has been discovered about brain
functioning. This coupled with the brains’ amazing ability to develop based on experience, whether that be initial
development, or reorganization following damage, provides increasing interest in OT theory and intervention.
These changes in neuroscience require an updating of our theories to incorporate the new findings in order to
facilitate acceptance of our unique perspective on central nervous system functioning as it relates to human
occupation.
The following is a brief literature review of the concept of sensory modulation within the field of occupational
therapy. This review begins with the seminal work of Ayres and traces the contributions of many outstanding
occupational therapy researchers and theoreticians over the years in operationalizing the concept of sensory
modulation.
Ayres on modulation
Ayres defined sensory integration as, "the neurological process that organizes sensation from one’s own body
and from the environment and makes it possible to use the body effectively within the environment. The spatial
and temporal aspects of inputs from different sensory modalities are interpreted, associated, and unified" (Ayres,
p. 11, 1989). Over the course of her career, Ayres conceptualized a number of disorders related to disrupted
sensory processing. She empirically identified several clusters of behaviors related to specific patterns of test
scores and observations. The interpretation of these patterns was based on Ayres’ theory of sensory integration.
At the time, Ayres referred to two broad categories of sensory processing (discriminative and protective).
In Ayres’ view, sensory discrimination leads to perception, conceptualization, and action. Ayres’ research
delineated the role of discriminative sensory processing in the development of functions such as body scheme,
smooth accurate movement, bilateral skill, visual perception and praxis.
In terms of modulation, Ayres discussed the balance of both inhibitory and excitatory influences on the brain.
According to Ayres, "the combination of facilitatory and inhibitory messages produces modulation which is the
nervous system’s process of self organization" (1979, p. 44-45). "Modulation is the process of increasing or
reducing neural activity to keep that activity in harmony with all the other functions of the nervous system"
(Ayres, 1979, p. 70). Ayres defined modulation as the "brain’s regulation of it’s own activity" ( 1979, p. 182). It
involves facilitating some neural messages to produce an enhanced response and inhibiting other messages to
reduce activity. She highlighted the role of the vestibular system in modulating the activity of the other systems.
The central connections of the vestibular system place it in a key position to modulate activity in the brain stem,
cerebellum, and related ascending pathways.
Over the course of rigorous theory development, Ayres elegantly ascertained several clusters of sensory
processing phenomenon and behavioral symptoms. One cluster that emerged from Ayres’ factor analytic studies
included tactile defensiveness and hyperactivity. Ayres introduced the concept of tactile defensiveness as
avoiding or negative reactions to non-noxious tactile stimuli (Ayres, 1964). She conceptualized tactile
defensiveness as an imbalance between discriminative and protective sensory processing. While the concept of
tactile defensiveness received the bulk of the attention, Ayres also suggested that hypersensitivities might be
observed in other sensory modalities. Ayres is also responsible for coining the terms gravitational and postural
insecurity.
Based on a 1980 study of children with autism, Ayres and Tickle suggested that "children who register sensory
input but failed to modulate it responded better to therapy than those who were hypo-responsive or failed to
orient to sensory input" (p. 375, 1980). They described this failure to orient as inadequate registration of
incoming sensory stimuli. They further proposed that SI treatment, "was more effective in modulating sensory
input than in helping the brain to register or orient to it" (Ayres, & Tickle, p. 381, 1980).
A central tenant of Ayres conceptualization of sensory integration was the premise of the brain’s ability to
regulate its own activity. A classic SI approach utilizes this principle in concert with other guiding principles which
include the idea that the treatment must be child-directed, with the therapist guiding the just right challenge in
order to facilitate adaptive responses. These core principles guide clinical reasoning and continued theory
building in the area of sensory integration.
Knickerbocker
In her 1980 book, A Holistic Approach to Learning Disorders, Barbara Knickerbocker expanded Ayres’ concept
of tactile defensiveness to a broader category of sensory defensiveness. Knickerbocker placed sensory
defensiveness on a continuum with sensory dormancy. She described sensory dormancy as, "too
much…inhibition of incoming sensory stimuli" (p. 32). She continued Ayres’ conceptualization of defensiveness
as an imbalance of inhibitory and excitatory forces. In Knickerbocker’s view, too little inhibition resulted in
sensory defensiveness and too much inhibition resulted in sensory dormancy.
Dunn and Fisher
In a pair of articles, Ann Fisher and Winnie Dunn (1983; Dunn & Fisher, 1983) proposed a concept that
influenced thinking regarding SMD for many years. They proposed that tactile defensiveness and registration
problems were the opposing ends of a single continuum. They cite Ayres for suggesting the notion of registration
as an emerging, important clinical concept. This was based on the work of Pribram and colleagues (Pribram &
McGinnis, 1975). Dunn & Fisher concretized the notion of registration and dichotomously contrasted it with
defensiveness. This continuum notion became the central tenant of thinking about sensory modulation for the
next decade.
Cermak
The state of knowledge regarding modulation of sensation was in its infancy during the 1980’s. Toward the end
of this period, Sharon Cermak wrote a two part series for the AOTA (American Occupational Therapy
Association) Sensory Integration Special Interest Section Newsletter, on the role of sensory integration in
understanding and treating attention deficits (Cermak, 1988). In pediatric occupational therapy, the SIS
Newsletters have traditionally provided an excellent forum for fostering clinical reasoning and promoting
communication between research and practice. This article served both of these purposes, and continues to
provide an important summative backdrop for current thinking about sensory modulation. In this set of articles,
Cermak summarized tenets of sensory modulation from within the field of OT as well as bridging the gap of
knowledge regarding the relevant issues from outside of the field of OT.
Cermak provided a valuable summary of perspectives on arousal and attention from researchers outside of the
field of OT. She included in this paper a presentation of a working model of the multiple continuums that play a
role in arousal and attention mechanisms. Each offered separate linear continuums of various aspects of
processing related to attention and arousal as follows:
Kinsbourne’s (1987) continuum opposes underfocused attention and hyperactive behavior with overfocused
attention and overanxious behavior. Zentall and Zentall’s (1983) arousal continuum, comprising low to high
CNS arousal in a linear relationship. Porges’ (1976) ANS continuum, with polar relations between
parasympathetic and sympathetic divisions. Each of these continua portray a linear relationship. What is
interesting about this theory period is that each of the versions discuss different aspects of processing, and yet
theorizing within the field of OT continued to lump these together into one broad linear continuum. The OT
models attempted to capture the essence of each of the separate continua but in so doing reduced the
complexity of neural function into a model that while simple, was inaccurate. This served an initial purpose of
providing a framework for thinking about SMD. However, as Cermak’s review highlights, any simple, linear
conceptualization while appealing, is misleading.
Fisher, Murray and Bundy
As a new decade unfolded, so did thinking about SMD. Fisher, Murray and Bundy, in their 1991 text, Sensory
Integration Theory and Practice, included SMD in a revised version of the classic Ayres sensory integration flow
chart. In their description of disorders in sensory modulation, Fisher, Murray and Bundy, included aversive
responses, gravitational insecurity, sensory defensiveness and tactile defensiveness. The major observable
behavioral signs of SMD-- avoidance, distractibility and increased activity level--were suggested as the end
products of such a disruption (Fisher, Murray and Bundy, 1990).
Lane and Royeen
Royeen (1989) elaborated on a continuum model where sensory defensiveness and sensory dormancy,
together, can be considered sensory modulation disorders and are on opposing ends of a sensory
responsivity/registration continuum with over orientation at one end and a failure to orient on the other end.
Royeen further noted that this continuum might in fact be circular with sensory dormancy and defensiveness as
potentially adjacent functions.
Royeen and Lane (1991) advanced the notion of a midrange between the hyper and hypo responsive ends of
the linear continuums. They described individuals who had difficulty achieving mid-range responses on the
defensiveness-dormancy continuum. Royeen and Lane describe the concept of deficiencies in the modulation of
sensation as being key to explaining sensory defensiveness and sensory dormancy. This was in contrast to
simply considering poor inhibition, which traditionally had been the mechanism used to explain SMD in previous
OT models.
Koomar and Bundy
Koomar and Bundy (1991) state, "when an individual overresponds, underresponds or fluctuates in response to
sensory input in a manner disproportional to that input, we say that the individual has a sensory modulation
disorder" (p. 268, 1991). They also describe a complex condition, which paradoxical to a continuum model,
allows for an individual to have problems with both discrimination and modulation of sensation. Their chapter
also provided a nice overview of treatment approaches for tactile defensiveness, gravitational insecurity,
aversive responding to movement, and poor registration.
Wilbarger & Wilbarger
Wilbarger & Wilbarger (1991) promote the concept of sensory defensiveness as consistent with normal
defensive responses. They propose that sensory defensiveness is on a continuum of approach and avoidance
behaviors. This is in direct contrast to the sensory defensiveness/poor registration continuum promoted by other
theorists. The Wilbargers’ suggest that sensory defensiveness is one of a subset of sensory modulation
disruptions.
Kimball
Kimball (1993) describes sensory modulation problems in terms of the arousal state created due to the
influences of sensation. "Persons who have sensory system modulation problems have more changeable
arousal or reaction levels than normal. This results in problems with adaptive responses because there systems
lack stability" (p 96-97). Kimball related these behavioral phenomenon to the classic inverted U shaped curve
(Hebb, 1949), highlighting an important concept that "sensory system modulation fluctuates within a range of
normal,"(p. 98). In this conceptualization, performance and adaptive capacity are poor at both low and high level
of arousal. In the middle ranges of arousal, performance and adaptation are optimal. Additionally, Kimball
reiterated the notion that a single sensory system may not be isolable, "sensory systems do not function
independently. Arousal in several systems can combine" (p. 97, 1993).
Importantly, Kimball also introduced the concept of shut down which she described as a protective mechanism
against severe overload. She illustrated the notion of a non-linear continuum by describing individuals at the
extremes of behavior i.e., "some children even react in a dangerous way and go from overarousal to
physiological shut down."
Parham and Mailloux
Parham and Mailloux (1996) define sensory modulation as "a tendency to generate responses that are
appropriately graded in relation to incoming sensory stimuli rather than under reacting or overreacting to them."
They support the views expressed by Cermak (1988) and Royeen (1989) that modulation disorders are
represented by a continuum from registration problems to sensory defensiveness. They describe dysfunction as
either fluctuations or a tendency to function at one extreme or the other. They further describe sensory
registration problems as a failure to attend to or register relevant environmental stimuli. Parham and Mailloux
note that registration problems are often seen in children with autism and developmental delays. Usually more
than one sensory system is involved, but there are inconsistencies such as ignoring "relevant stimuli while
overfocusing on irrelevant stimuli" (p. 324), or "to lack sensory registration in some situations but react with
extreme sensory defensiveness in others" (p. 324). Children lacking appropriate registration may engage in
intense or dangerous behaviors. They also describe a situation where lack of registration creates a lack of inner
drive to engage in typical childhood occupations and is detrimental to long term development.
Empirical work currently shaping the concept of SMD
At present, there are a number of researchers endeavoring to expand our knowledge regarding disruptions in
sensory processing.
Winnie Dunn and her colleagues have been developing a normed parent questionnaire, the Sensory Profile
(Dunn & Westman, 1997). An analysis of the responses made by parents of typical children on the 125 items
revealed nine factors related to sensory integration some of which reflect sensory modulation and reactiveness
(Dunn & Brown, 1997). These factors include sensory seeking, emotional reactivity, low endurance/tone, oral
sensitivity, inattention/distractibility, poor registration, sensory sensitivity, sedentary, and fine motor/perceptual.
Dunn further has suggested that sensory modulation needs to be considered on the multiple dimension of a
person’s threshold for sensory events and responsiveness to sensation (Dunn, 1997).
Several researchers have been working to understand further the nature of sensory defensiveness. This
collection of work is beginning to verify long held clinical opinions that disruptions in sensory modulation are
identifiable phenomenon that effect the daily lives of individuals. Moya Kinneally and her colleagues have been
studying the phenomenology of sensory defensiveness in adults. They have conducted several studies on the
association of sensory defensiveness and anxiety, depression, locus of control orientation, and perception of
pain in typical adults. They have also explored treatment of sensory defensiveness using a sensory diet model,
in the tradition of the Wilbarger approach. Grace Baranek and her colleagues have conducted a series of studies
(Baranek & Berkson, 1994; Baranek, Foster & Berkson, 1997) to understand the role of sensory defensiveness
in individuals with developmental disabilities and autism. Between 3-30 % of their sample of individuals with
developmental disabilities had sensory defensiveness. She also provides supporting evidence for sensory
defensiveness as a unifying construct, and within this, her evidence suggests that there may be smaller subsets
of modality specific disruptions, such as auditory sensitivity. These studies are adding to the body of
understanding that sensory defensiveness may be a unique disruption of sensory modulation. As such, it
appears to be a legitimate phenomenon and not necessarily a by-product of another disorder.
Recent work by Lucy Miller and colleagues at The Children’s Hospital in Denver has begun to quantify the notion
of sensory modulation through the use of psychophysiological measurement of sensory reactivity. In a series of
articles (Miller & McIntosh, 1998; Miller et al, in press), Miller has identified patterns of unusual sensory reactivity
in a variety of groups. These studies are providing some interesting insights that support continued efforts to
conceptualize and quantify disruptions in sensory modulation.
Conclusions and Future Directions
Just as the early work of Ayres included syndrome validation, the on-going research of Dunn, Kinnealey,
Baranek, Miller, and others is beginning the process of validating the concept of SMD.
The review presented here summarizes the primary notions related to the concept of sensory modulation within
the field of occupational therapy. The early work of Ayres began this endeavor with her findings of the
noteworthy cluster of tactile defensiveness and hyperactivity. This was followed by the multiple discussions of
how a single continuum might describe the clinical presentation of poor modulation. However, recent work is
beginning to question this limited concept. Dunn has suggested that there are probably multiple, interacting
continua. Clearly, the brain is a complex heterarchy. As such, any model trying to solidify a brain-behavior
relationship must reflect that complexity. Therefore, the future of sensory modulation will probably include
complex models comprised of dynamic, interactive systems.
Two important concepts of modulation that have been reviewed in this article relate to the ideas of sensory
reactivity and optimal arousal. At this point in the OT literature, there is not a model of sensory modulation that
incorporates both of these concepts in concert. This important step needs to be taken in order to move the
theory of SMD forward.
In our review of the literature, we have been unable to discover a satisfying definition of sensory modulation. We
therefore propose the following conceptualization of sensory modulation as useful in considering the complexity
of processing and behavior involved.
Sensory modulation is the intake of sensation via typical sensory processing mechanisms such that the degree,
intensity and quality of response is graded to match environmental demand and so that a range of optimal
performance/adaptation is maintained.
While the linear continuum models that have been the dominant means of conceptualizing SMD served an
important purpose, it is apparent that the nervous system mechanisms that support modulation are many, varied
and complex. As such, a new model that captures the dynamic, interacting networks is required. Moreover,
within the field of occupational therapy, research regarding the occupational nature of SMD should be initiated.
About the Authors
Tracy Stackhouse, OTR, received her degree in OT from Colorado State University. She is SIPT certified and
NDT trained. She worked for nearly a decade as the clinical specialist in sensory integration at the Children’s
Hospital in Denver, and as the OT for the Fragile X Syndrome Treatment Center. She is currently working on her
Ph.D. in developmental cognitive neuroscience with Dr. Bruce Pennington at the University of Denver.
Tracy can be contacted through e-mail at: [email protected]
Julia Wilbarger, MS, OTR, received a B.S. in physiological psychology from the University of California, Berkeley
and a M.S. in Occupational Therapy from Boston University. She has worked as an occupational therapist in
early intervention with high risk and developmentally delayed infants and toddlers, in private practice and the
public schools. Julia was the clinical specialist for the sensory integration team at the Children’s Hospital in
Denver for several years. She is the co-founder of Avanti, a sensory integrative summer camp and was the
administrative director of that project for several years. Julia lectures nationally and internationally on sensory
defensiveness and has served on the Sensory Integration Special Interest Section Standing Committee of the
AOTA. She is currently in a doctoral program at the University of Denver, Colorado.
Julia can be contacted through e-mail at: [email protected]
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Revised September 12, 1998 Copyright 1998 - The KID Foundation, 1901 West Littleton Blvd., Littleton, CO
80120
Last Updated ( Saturday, 17 June 2006 )