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Sensory Integration, Sensory Processing, and Sensory Modulation Disorders: Putative Functional Neuroanatomic Underpinnings

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Sensory Integration, Sensory Processing, and Sensory Modulation Disorders: Putative Functional Neuroanatomic Underpinnings Cerebellum DOI 10.1007/s12311-011-0288-8 Sensory Integration, Sensory Processing, and Sensory Modulation Disorders: Putative Functional Neuroanatomic Underpinnings Leonard F. Koziol & Deborah Ely Budding & Dana Chidekel # Springer Science+Business Media, LLC 2011 Abstract This paper examines conditions that have vari- We present likely etiologies for these symptoms, not only ously been called sensory integration disorder, sensory as they drive neurodevelopmental pathologies but also as processing disorder, and sensory modulation disorder (SID/ they can be understood as variations in the development of SPD/SMD). As these conditions lack readily and consis- neural networks. tently agreed-upon operational definitions, there has been confusion as to how these disorders are conceptualized. Keywords Sensory integration disorder . Sensory Rather than addressing various diagnostic controversies, we modulation disorder . Sensory processing disorder . Basal will instead focus upon explaining the symptoms that are ganglia . Cerebellum believed to characterize these disorders. First, to clarify the overall context within which to view symptoms, we summarize a paradigm of adaptation characterized by Introduction continuous sensorimotor interaction with the environment. Next, we review a dual-tiered, integrated model of brain This paper examines the putative neuroanatomic underpin- function in order to establish neuroanatomic underpinnings nings of conditions variously called sensory integration with which to conceptualize the symptom presentations. disorder (SID), sensory processing disorder (SPD), and Generally accepted functions of the neocortex, basal sensory modulation disorder (SMD). The term “sensory ganglia, and cerebellum are described to illustrate how integration” was originally proposed by Ayers [1, 2]. The interactions between these brain regions generate both term was introduced to identify a field of study focusing adaptive and pathological symptoms and behaviors. We upon individuals—primarily children—who demonstrated then examine the symptoms of SID/SPD/SMD within this atypical behavioral responses to sensory stimulation. This interactive model and in relation to their impact upon the clinical condition is now referred to as SPD. SMD can be development of inhibitory control, working memory, considered as a specific subtype of SPD, in which hypo and/ academic skill development, and behavioral automation. or hyperresponsiveness to sensory stimuli is emphasized [3]. These conditions, to which we will refer to as SID/SPD/ SMD hereafter, are primarily diagnosed through interviews The authors wish to acknowledge Jessica Chang for her research and observational rating scales [4]; however, the diagnosis is assistance. controversial. While Regulation Disorders of Sensory Pro- L. F. Koziol cessing are included in the Diagnostic Classification of Chicago, IL, USA Mental Health and Developmental Disorders in Infancy and e-mail: [email protected] Early Childhood [5], neither SID, SPD, nor SMD is listed in D. E. Budding (*) the DSM-IV or ICD-9 nor were the apparently unique Manhattan Beach, CA, USA behavioral symptoms that define these conditions included as e-mail: [email protected] criteria for any DSM-IV or ICD-9 diagnosis. At the time of ’ D. Chidekel this paper s writing, there is continuing debate as to whether Tarzana, CA, USA or not SPD will be included in the DSM-V. Cerebellum Thus far, the symptoms of SPD have not been variables interfere with the child’s ability to effectively participate in of interest in the fields of psychiatry, neuropsychiatry, or childhood activities in order to make the diagnosis rather neurology. The Handbook of Pediatric Neuropsychology than the presence or absence of a single symptom in an makes no mention of these conditions, while the symptoms effort to limit false positive diagnoses. that are considered to comprise these disorders are only The Sensory Profile defines aspects of sensory process- briefly mentioned in a short discussion of developmental ing disorders within four clusters or constructs, but dyspraxia [6]. Presently, SID/SPD/SMD only appear in the identifying clusters or groups of symptoms is not the same diagnostic nomenclatures of the professions that identify as identifying the neuroanatomic underpinnings that drive them, specifically, the fields of occupational and sometimes them, nor does identifying clusters or symptom groups physical therapy. At the same time, the wide range of clarify brain–behavior relationships. In this way, The symptoms that characterize these conditions very clearly Sensory Profile is akin to the DSM and ICD systems in overlap with disorders diagnosed in other behaviorally that it represents a behaviorally defined nomenclature and defined systems. As such, while the behaviors that not one that is neuroanatomically organized. Just as most characterize SPD are not variables of interest within the conditions listed in the DSM are characterized by abnor- framework of widely accepted diagnostic nomenclatures, malities in multiple brain regions [8], it is likely that the this should not imply that the behaviors are insignificant or varying presentations of SID/SPD/SMD are characterized unimportant. Nevertheless, the validity of the constructs by anomalous functioning in multiple brain regions and used to define SPD bear consideration, as do the relation- mechanisms as well. Our purpose is not to criticize the ships between known neuroanatomical structures and Sensory Profile or any other behaviorally defined diagnos- neurodynamic processes and the behaviors that characterize tic system. Our purpose is to clarify the neuroanatomic these conditions. frameworks underlying symptom presentations to facilitate The meaning of the term “sensory” in SID/SPD/SMD communication among disciplines. needs to be clarified first. The Sensory Profile question- In this review, we will differentiate behaviors frequently naire, which is perhaps the most commonly used observa- associated with SID/SPD/SMD into several categories. We tional rating scale to make this diagnosis, does not conceptualize all behavior as inherently requiring an operationally define “sensory processing” nor does it integration of sensory input with motor output and we provide a unifying underlying neuroanatomic construct to operate from a perspective strongly biased toward placing explain it [4]. At the same time, the instrument encom- behavior in a context of continuous sensorimotor interac- passes behaviors that seem to go beyond the scope of tion between an individual and his/her environment [9]. “sensory processing,” and it refers to categories or Our categories will include factors involved in the behaviors and behavioral observations that are multi- perception, processing—or “noticing”—of sensory experi- factorial or multiply determined. For example, some ences, the modulation of these experiences as characterized sections of the Sensory Profile refer to auditory, visual, by hyper- and hypo-sensitivities (and as observationally tactile, oral, and multisensory processing within these manifested by hyper and hypo-responsiveness), and the modalities, while others refer to sensory modulation and cognitive and behavioral symptoms that can be generated relate it to “endurance and tone,” body position and by disturbances within sensory systems. We will address movement, and affect and emotional responsiveness. There these issues within the context of a neuroscientific is a section in which emotional and social responses are knowledge base. rated and another that assesses presumed, predicted The brain’s functional architecture evolved to meet the behavioral outcomes of sensory processing [3]. Some of needs of interactive behavior; this evolutionary trend was the symptoms listed overlap with behaviors that are strongly conserved during phylogeny. We thus do not included in the diagnostic categories of the DSM. endorse a simplified, serial information processing frame- This complex combination of factors suggests that the work that posits: First, we perceive; then we think to Sensory Profile cannot be measuring a monolithic construct organize a response; then we respond. Seminal papers by or “one thing.” In fact, James and colleagues recently Cisek and Kalaska [9], Shadlen and Movshon [10], and recognized the heterogeneity of these symptom presenta- Singer [11] review neurobiologic data from various tions and identified two subtypes of SMD characterized by disciplines and conclude that there is little evidence to externalizing and internalizing behavioral presentations, support a perception–cognition–action model as a phyloge- respectively [7]. Some of the symptoms listed in the netically conserved or useful primary mode of adaptation Sensory Profile are vaguely defined and are observed in [9–11]. Rather, we endorse a sensorimotor interaction most children at least some of the time, which can lead to paradigm that challenges traditional models of perception, over-diagnosis of the condition. The Sensory Profile cognition, and behavior by stressing the significant overlap requires the identification of a group of behaviors that and interaction between cortical and subcortical regions that Cerebellum serve both consciously controlled and automatic adaptive and/or hypersensitivity (responsiveness) to sensory stimu- behaviors as they occur in “real time” [12, 13]. This lation is estimated to occur in 5% of children within the sensorimotor interaction paradigm also challenges the general population, while
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