Lucy Jane Miller
Elysa J. Marco
Robyn C. Chu4,5
Stephen Camarata- 1Department of Pediatrics (Emeritus), University of Colorado, Denver, CO, United States
- 2Sensory Therapies and Research Institute for Sensory Processing Disorder, Centennial, CO, United States
- 3Cortica (United States), San Diego, CA, United States
- 4Radiology & Biomedical Imaging, University of California San Francisco, San Francisco, CA, United States
- 5Growing Healthy Children Therapy Services, Rescue, CA, United States
- 6School of Medicine, Vanderbilt University, Nashville, TN, United States
Editorial on the Research Topic
Sensory Processing Across the Lifespan: A 25-Year Initiative to Understand Neurophysiology, Behaviors, and Treatment Effectiveness for Sensory Processing
Growing Scientific Knowledge in Sensory Processing
The Growth of Science
Science must evolve. Kuhn (1970) proposed that scholars adapt their research as new information is discovered and described how the growth of knowledge results in paradigm shifts. Science advances in increments based in part on fact, law, and theory and in part on imagination, hypothesis, and error. The articles in this issue demonstrate Kuhn's premise and the need for rigorous, multidisciplinary, empirical research to underlie a new field such as sensory processing.
Brief History of SPD
Ayres (1972) was the first to explore sensory processing, focusing on children with learning disorders. In impressive detail, she collected and studied clinical observations, standardized assessment data, and treatment methods. She proposed a new syndrome, which she termed “sensory integration dysfunction” (SID). From 1964 to 1966, Ayres, an occupational therapist, conducted post-doctoral studies at UCLA Brain Research Institute. Membership in the neuroscience department permitted Dr. Ayres to learn the culture of research in a transdisciplinary environment and to hypothesize the brain/behavior connection in the newly conceptualized condition.
This issue of Frontiers celebrates the growth of scientific knowledge, founded upon Ayres' research from 1960 to 1988 (Ayres, 1955, 1964, 1966a,b; Ayres, 1971, 1977, 1989) and progressing with the support of a 25-year initiative, by the Wallace Research Foundation (WRF) (1994–2019). The WRF funded over 50 scholars, who, as members of the SPD Workgroup, worked for two decades to evaluate whether the reliability and validity of sensory processing issues were strong enough to suggest a new syndrome, which was termed Sensory Processing Disorder (SPD).
Breadth of Knowledge Gained
Articles in this issue of Frontiers represent many of the latest studies in SPD research and represent the ripple effect as discussed in Kuhn's premise; that is, Ayres' early work led to the science conducted by the WRF SPD workgroup and many other important researchers in the field. We review the scientific breakthroughs that have occurred in the past quarter-century and propose a theoretical model that may be helpful to future researchers trying to specify the reliability and validity of SPD as a new syndrome (Pennington, 1991). While not exhaustive of the work in sensory processing done by the neuroscience and occupational therapy communities as a whole, the framework below represents the five areas in Pennington's model of syndrome validation. For the interested reader, we have included multiple citations for publications funded by the WRF below.
Etiology and Epidemiology
Ahn et al. (2004), reported that 13% of kindergarten parents indicated significant sensory challenges. As this was derived from a 40% response rate, the estimate of SPD prevalence in a community sample was 5%. Ben-Sasson and Carter et al. (Ben-Sasson et al., 2009, 2010; Carter et al., 2011), furthered this inquiry by assessing SPD in a 10-year, prospective study of all births in New Haven, Connecticut. In children up to 8 years of age, 16% had symptoms of SPD, with 75% reporting no additional mental health diagnosis. In addition, Goldsmith et al. (Keuler et al., 2011; Van Hulle et al., 2012, 2015, 2018, 2019), conducted elegant twin studies concluding that sensory symptoms occur significantly more often in identical than in fraternal twins, implicating a genetic link. These studies were pivotal in shaping the landscape of this condition and highlighting the need for further etiological studies.
Pathogenesis
Over the past two decades, we have furthered our understanding of the neurophysiology of sensory processing in general, however additional research is needed for specific subtypes of the condition. For example, Miller et al. (McIntosh et al., 1999; Miller et al., 1999) contributed that children with SPD show increased electrodermal responses and decreased habituation while Davies and Gavin (Davies and Gavin, 2007; Brett-Green et al., 2008; Davies et al., 2009, 2010; Gavin et al., 2011; Chang et al., 2012; Brett et al., 2016; Lagasse et al., 2019; Crasta et al.) found evidence of reduced sensory gating. Utilizing rodent models to better understand the mechanisms of these electrophysiologic differences, Bauman, Levin and colleagues (Levin et al., 2005, 2007; Schmajuk et al., 2006, 2009; Roegge et al., 2007; Larrauri and Levin, 2012; Mahendra et al., 2012; Skefos et al., 2014; Larrauri et al., 2015; McMahon et al.) determined that sensory gating deficits were related to activity of cholinergic, glutamatergic, and adrenergic receptors which suggests potential therapeutic approaches.
Animal studies have also greatly contributed over time to our understanding of the interplay of information among the individual sensory streams and multisensory integration. For over 20 years, Schneider et al. (Schneider et al., 1991, 2007, 2008, 2009, 2011, 2013, 2017; Moore et al., 2008; Coe et al., 2010; Converse et al., 2013; Schneider et al.), studied Rhesus monkeys. With positron emission tomography (PET) imaging, Schneider's findings suggest that SPD affects dopamine (DA) pathways, resulting in decreased regulation of sensory and affective processes and increased over-responsivity to stimuli. Stein and Rowland et al. (Stein, 1998, 2012; Fuentes-Santamaria et al., 2008, 2009; Stein et al., 2009; Yu et al., 2009, 2010; Cuppini et al., 2010, 2018; Rowland et al., 2014; Xu et al., 2015; Miller et al., 2017), have informed the field regarding the importance of the superior colliculi as a multisensory integrating region. In feline models, they found that simultaneous auditory-visual exposure radically changes input to neurons, honing the cat's ability to detect, identify, and respond to environmental events.
This understanding was then applied to children with autism and SPD by Molholm and Foxe who show that children with sensory over-responsivity have reduced auditory-visual integration affecting their perception of speech in noisy environments. Marco and Mukherjee's (Marco et al., 2011, 2012, 2018; Owen et al., 2013; Wickremasinghe et al., 2013; Mukherjee et al., 2014; Chang et al., 2016; Demopoulos et al., 2017; Brandes-Aitken et al., 2019; Payabvash et al., 2019; Tavassoli et al., 2019) structural neuroimaging work revealed that children with SPD show decreased white matter connectivity predominantly in the posterior brain regions that correlates with sensory function and has elements that are overlapping and some that are distinct from an autism cohort. They also show that there is a significant overlap in visual motor control and cognitive control deficits in children with SPD which result from disruption of shared white matter tracts (Brandes-Aitken et al., 2018, 2019). Additional work by Marco and Nagarajan et al. (Demopoulos et al., 2017), using magnetoencephalographic functional imaging suggests that children with SPD show an intermediate phenotype with regard to the time course of somatosensory (tactile) processing relative to children with autism spectrum disorders (ASD) and neurotypical controls.
Phenotype
Phenotype (core and secondary symptoms) exploration of sensory over-responsivity, also termed hyper-reactivity or sensitivity, has been researched in otherwise neurotypical individuals or in cohorts with additional mental health conditions (Miller et al., 2009; Schoen et al., 2009, 2014a; Tavassoli et al., 2018). Cermak et al. (Zobel-Lachiusa et al., 2015; Bar-Shalita and Cermak, 2016; Chistol et al., 2018; Ben-Sasson et al., 2019; Kilroy et al., 2019), measures aversive sensory responsiveness in individuals with autism and in the general population, concluding that sensory responsiveness has high correlation to pain perception. Ben-Sasson et al. suggest that slow sensory habituation may underlie over-responsivity in individuals with obsessive compulsive disorder. In addition to electroencephalographic studies cited above, Gavin and Davies discuss attention and sensory profiles in children with SPD and ASD. They successfully categorize 76.8% of participants (SPD vs. ASD vs. Typical) for group membership based on standardized test scores.
There are various assessment tools utilized for determining the extent of sensory processing dysfunction, with parent report measures, the Sensory Profile 2 and Sensory Processing Measure (Diane Parham et al., 2007; Winnie Dunn, 2014), being the most commonly used in research, clinics, and schools. There are excellent reviews for more in depth coverage of this important topic (Eeles et al., 2013; Yeung and Thomacos, 2020). None of the current assessments evaluate all domains thought to be related to sensory processing. The development of a standardized direct assessment tool with psychometric data for multiple facets of sensory processing (sensory modulation, sensory-based motor, and sensory discrimination) is important to future research and clinical phenotyping. The Sensory Processing Three Dimensions Measure (SP3D) (Lane et al., 2000; Miller and Lane, 2000; Miller et al., 2001, 2007a; Schoen et al., 2008, 2014b, 2017) is one of the assessments being developed to fill the need since the previous standardized scale (Ayres, 1989) is no longer published. Miller, Schoen and Mulligan (Miller et al., 2020a) are completing national standardization of the SP3D and Schoen et al. (Schoen et al., 2008, 2014b, 2017; Mulligan et al., 2019a,b), have contributed articles on this topic. Future research will use these comprehensive assessments to connect the phenotypic information to neuroimaging, leading to deeper understanding of sensory processing. Moreover, there is an ongoing need to further develop the phenotype and to specify the unique and shared features with other established phenotypes (e.g., ASD, Developmental Language Disorder, see Skuse, 2000). The continued refinement (and precision) for an SPD phenotype (or phenotypes as the data may ultimately show), is foundational for advancing the knowledge base to inform future behavioral, genetic, neurological and treatment research.
Treatment Effectiveness
Miller et al. (2007b), conducted a pilot randomized controlled trial (RCT) of treatment using occupational therapy for children with sensory modulation disorder and found improvement in personalized goals, attention and social function based on the Leiter International Performance Scale-revised. Schoen et al. (2018), reports sensorimotor and adaptive function improvement based on a chart review of 179 children receiving occupational therapy. Miller et al. (Miller et al., 2018, 2020b; Schoen et al., 2019), discuss a comprehensive new treatment based on these findings and clinical observations, which uses a sensory and relationship-based approach, the STAR Frame of Reference©. Pfeiffer et al. (2011) compared fine motor treatment vs. sensory integration (SI) therapy for children with ASD and showed additional benefit from SI for autism mannerisms and personalized goals. Similarly, Schaaf et al. (2014) assessed children with autism comparing SI with “usual care” and reported benefits for personalized goals, self-care and socialization. In this journal, Camarata and colleagues review the sensory integration treatment and other treatment issues including: (1) clinical trials and methods used in applied behavior analysis, (2) the neural-scientific paradigm of multisensory processing, and (3) controlling for potential confounds (Camarata, 2014a,b; Stevenson et al., 2014a,b,c; Davis et al., 2015; Stevenson et al., 2016). Additionally, a WRF-funded project investigating the role of brain training for cognitive control in children with SPD has contributed to the first digital therapeutic device for attention (EndeavorRX) being approved by the United States FDA (Anguera et al., 2017).
Developmental Course
There is a dearth of longitudinal work investigating sensory processing, including multisensory integration, across early development and with aging. McKibbon et al., study the trajectory of SPD by examining a sample of 231 adults who had emotion regulation difficulties that were preceded by SPD in childhood. This study opened up examination of the developmental trajectory of SPD, suggesting that SPD has a childhood onset and discussing possible mechanisms that might be involved in the progression. Concluded was that childhood SPD predicts Anxiety Disorder in adults defined by difficulties with emotion regulation, mediated by adult SPD symptoms. The article by Tavassoli et al. (2014) looking at sensory symptoms in adults with SPD and Autism further explores this hypothesis. Ben-Sasson et al. (2010) followed 521 children from infancy to 8 years old and concluded that early sensory sensitivities were associated with sensory over responsivity at school age. Ben-Sasson et al. (2019) recently completed a meta-analysis of sensory symptoms in children with ASD throughout the lifespan, with various studies with findings that sensory symptoms can increase, decrease, or be stable throughout the lifespan and calling for additional research to look more in depth at the moderating effects of age.
Value of Empirical Data for Change and Future Research
When defining a new science, reliable quantitative benchmarks often do not exist as was true with SPD. Thus, continuing definition is required. Conceptualization of the field grows as empirical data is obtained. This results in changes in theories and affects practice significantly. With the WRF initiative and world-wide study, each project increased knowledge incrementally, and the collaborative effect overall substantially expanded the understanding of SPD as a brain-based disorder.
Finding that the binary conception of SPD as a “disorder” was too simple, we view SPD not as a singular entity, but rather, a continuum of function-to-dysfunction for any given individual, which indicates a “dimension” rather than a “disorder”).
In the next quarter century, research will question brain networks, neurochemistry, and neural firing that explains the facets of disrupted sensory processing, from:
• Low-level abilities (perceive, protect, and react) to
• Mid-level processing (integrate, process, and relay) to
• High-level function (discriminate, plan, and respond).
With time and increased knowledge, adaptations to terminology have occurred. Naming SPD and categorizing the symptoms have validated parents' concerns and are partially related to including sensory hypo and hyper-reactivity as clinical constituents of autism spectrum disorders in the Diagnostic and Statistical Manual-5. Extensive research establishing the groundwork for additional studies has been accomplished and has provided a foundation for understanding that SPD is prevalent, diagnosable, and treatable. The WRF initiative, which we applaud and celebrate, has encouraged us to “keep in mind what is assumption and what is fact … [for] truth like infinity is to be forever approached, but never reached” (Ayres, abid, p. 4).
Author Contributions
All authors significantly contributed to the conception, data acquisition, drafting, and revision of the article.
Conflict of Interest
LM was the former director of the STAR Institute in Greenwood Village, CO. Much of the research described in the special issue was conducted while she was the director of the center and was compensated in that role. The center provides workshops, in-service training and direct client services for children with disabilities and their families. In addition, LM is an author on the Sensory Processing 3 Dimensions (SP3D), a commercially available assessment and as such, will receive royalties from Western Psychological Services, which will publish the test once data collection is finished and the examiner's manual is written (possibly 2024, depending when the COVID crisis is managed and testing can begin again). LM also receives royalties as the author of Sensational Kids, published by Penguin: NYC. Finally, LM was the awarded funding from the Wallace Research Foundation, which supported much of the research reported in this Frontiers special issue. None of the compensation was contingent upon any specific outcomes or findings from the research reported herein nor, for that matter, in any of LM research publications. None of the articles in this issue directly promotes any specific approach or product. EM is the executive director of neurodevelopmental medicine at Cortica Healthcare in San Rafael, CA where she provides clinical care, conducts research, and oversees the neurodevelopmental medicine faculty and support. She has received research funding from the Sensory Neurodevelopment and Autism Program crowdfunding campaign, UCSF RAP awards, the Wallace Research Foundation, as well as Akili Interactive. None of the compensation was contingent upon any specific outcomes or findings from the research reported herein nor, for that matter, in any of EM's research publications. EM also receives compensation from the National Institutes of Health for her participation in peer grant review. RC is the executive director of Growing Healthy Children Therapy Services in Rescue, CA where she is a treating occupational therapist, conducts research, provides consultation to other therapy practices, and teaches seminars in the community. She is on faculty for the STAR Institute where she teaches courses to therapists. She is a research consultant for UCSF and UCLA. None of her compensation in the aforementioned capacities, or any capacity, was contingent upon any specific outcomes or findings from the research reported herein, nor for that matter, in any of RC's research publications. SC receives salary support as a professor of Hearing and Speech sciences and a professor of Psychiatry at Vanderbilt University School of Medicine. He is a co-developer of conversational recast intervention and phonological recast intervention which are both evidence based Naturalistic Developmental Behavioral Interventions (NDBIs). SC's research is currently supported by grants from the National Institute on Deafness and Other Communication Disorders (NIDCD) and the National Institute on Mental Health (NIMH) of the NIH, the Institute of Educational Sciences (IES) of the US Department of Education, The National Endowment for the Arts (NEA), the Scottish Rite Mason's Foundation of Nashville. The Henry Wallace Foundation provided support for the research included in this special issue. He receives royalties for two books: The Intuitive Parent (2017) Penguin/Current and Late Talking Children: A Symptom or a Stage? (2014) MIT Press and is also coauthor of the Woodcock-Camarata Articulation Battery (WCAB, 2020) Schoolhouse Publications and receives royalties for this test. SC has no direct or indirect financial interest in the results presented herein other than to declare the research support provided by the Wallace Foundation.
Acknowledgments
A 25-year project, including over 50 people in multiple universities and countries is multi-faceted and complex. We wish to acknowledge and thank The Wallace Research Foundation whose vision for answers about sensory processing provided support for the studies described in this journal issue and more. Collecting and organizing the manuscripts was a collaborative team effort requiring ability and a desire to contribute to the mission of the project. I wish to acknowledge and thank the following professionals who checked content and format of the articles and assisted with the editorial and references. Without their devoted assistance this issue of Frontiers would not be a reality: Carol Stock Kranowitz, and Lisa Porter.
References
Ahn, R. R., Miller, L. J., Milberger, S., and McIntosh, D. N. (2004). Prevalence of parents' perceptions of sensory processing disorders among kindergarten children. Am. J. Occup. Ther. 58, 287–293. doi: 10.5014/ajot.58.3.287
Anguera, J. A., Brandes-Aitken, A. N., Antovich, A. D., Rolle, C. E., Desai, S. S., and Marco, E. J. (2017). A pilot study to determine the feasibility of enhancing cognitive abilities in children with sensory processing dysfunction. PLoS ONE. 12:e0172616. doi: 10.1371/journal.pone.0172616
Ayres, A. J. (1955). Proprioceptive facilitation elicited through the upper extremities: I. Background. Am. J. Occup. Ther. 9, 1–9.
Ayres, A. J. (1964). Tactile Functions. Their relation to hyperactive and perceptual motor behavior. Am. J. Occup. Ther. 18, 6–11.
Ayres, A. J. (1966a). Interrelations among perceptual-motor abilities in a group of normal children. Am. J. Occup. Ther. 20, 288–92.
Ayres, A. J. (1966b). Interrelationships among perceptual-motor functions in children. Am. J. Occup. Ther. 20, 68–71.
Ayres, A. J. (1971). Characteristics of types of sensory integrative dysfunction. Am. J. Occup. Ther. 25, 329–334.
Ayres, A. J. (1972). Sensory Integration and Learning Disorders. Los Angeles, CA: Western Psychological Services.
Ayres, A. J. (1977). Cluster analyses of measures of sensory integration. Am. J. Occup. Ther. 31, 362–366.
Ayres, A. J. (1989). Sensory Integration and Praxis Test (SIPT). Torrance: Western Psychological Services.
Bar-Shalita, T., and Cermak, S. A. (2016). Atypical sensory modulation and psychological distress in the general population. Am. J. Occup. Ther. 70:7004250010. doi: 10.5014/ajot.2016.018648
Ben-Sasson, A., Carter, A. S., and Briggs-Gowan, M. J. (2009). Sensory over-responsivity in elementary school: prevalence and social-emotional correlates. J. Abnorm. Child Psychol. 37, 705–716. doi: 10.1007/s10802-008-9295-8
Ben-Sasson, A., Carter, A. S., and Briggs-Gowan, M. J. (2010). The development of sensory over-responsivity from infancy to elementary school. J. Abnorm. Child Psychol. 38, 1193–1202. doi: 10.1007/s10802-010-9435-9
Ben-Sasson, A., Gal, E., Fluss, R., Katz-Zetler, N., and Cermak, S. A. (2019). Update of a meta-analysis of sensory symptoms in ASD: a new decade of research. J. Autism Dev. Disord. 49:4974–96. doi: 10.1007/s10803-019-04180-0
Brandes-Aitken, A., Anguera, J. A., Chang, Y. S., Demopoulos, C., Owen, J. P., and Gazzaley, A., et al. White matter microstructure associations of cognitive and visuomotor control in children: a sensory processing perspective. Front. Integr. Neurosci. (2019) 12:65. doi: 10.3389/fnint.2018.00065.
Brandes-Aitken, A., Anguera, J. A., Rolle, C. E., Desai, S. S., Demopoulos, C., Skinner, S. N., et al. (2018). Characterizing cognitive and visuomotor control in children with sensory processing dysfunction and autism spectrum disorders. Neuropsychology 32, 148–160. doi: 10.1037/neu0000404
Brett, B., Rush, S., Shepherd, J., Sharpless, N., Gavin, W., and Davies, P. (2016). A preliminary comparison of multisensory integration in boys with autism spectrum disorder and typically developing controls. Int. J. Neurol. Res. 2, 241–255. doi: 10.17554/j.issn.2313-5611.2016.02.45
Brett-Green, B. A., Miller, L. J., Gavin, W. J., and Davies, P. L. (2008). Multisensory integration in children: a preliminary ERP study. Brain Res. 1242, 283–290. doi: 10.1016/j.brainres.2008.03.090
Camarata, S. (2014a). Early identification and early intervention in autism spectrum disorders: accurate and effective? Int. J. Speech Lang. Pathol. 16, 1–10. doi: 10.3109/17549507.2013.858773
Camarata, S. (2014b). Validity of early identification and early intervention in autism spectrum disorders: future directions. Int. J. Speech Lang. Pathol. 16, 61–8. doi: 10.3109/17549507.2013.864708
Carter, A. S., Ben-Sasson, A., and Briggs-Gowan, M. (2011). Sensory over-responsivity, psychopathology, and family impairment in school-aged children. J. Am. Acad. Child Adolesc. Psychiatry. 50, 1210–1219. doi: 10.1016/j.jaac.2011.09.010
Chang, W. P., Gavin, W. J., and Davies, P. L. (2012). Bandpass filter settings differentially affect measurement of P50 sensory gating in children and adults. Clin. Neurophysiol. 123, 2264–2272. doi: 10.1016/j.clinph.2012.03.019
Chang, Y. S., Gratiot, M., Owen, J. P., Brandes-Aitken, A., Desai, S. S., Hill, S. S., et al. (2016). White matter microstructure is associated with auditory and tactile processing in children with and without sensory processing disorder. Front. Neuroanat. 9:169. doi: 10.3389/fnana.2015.00169
Chistol, L. T., Bandini, L. G., Must, A., Phillips, S., Cermak, S. A., and Curtin, C. (2018). Sensory sensitivity and food selectivity in children with autism spectrum disorder. J. Autism Dev. Disord. 48, 583–591. doi: 10.1007/s10803-017-3340-9
Coe, C. L., Lubach, G. R., Crispen, H. R., Shirtcliff, E. A, and Schneider, M. L. (2010). Challenges to maternal well-being during pregnancy impact temperament, attention, and neuromotor responses in the infant rhesus monkey. Dev. Psychobiol. 52, 625–37. doi: 10.1002/dev.20489
Converse, A. K., Moore, C. F., Moirano, J. M., Ahlers, E. O., Larson, J. A., Engle, J. W., et al. (2013). Prenatal stress induces increased striatal dopamine transporter binding in adult non-human primates. Biol. Psychiatry. 74, 502–510. doi: 10.1016/j.biopsych.2013.04.023
Cuppini, C., Stein, B. E., and Rowland, B. A. (2018). Development of the mechanisms governing midbrain multisensory integration. J. Neurosci. 38, 3453–3465. doi: 10.1523/JNEUROSCI.2631-17.2018
Cuppini, C., Ursino, M., Magosso, E., Rowland, B. A., and Stein, B. E. (2010). An emergent model of multisensory integration in superior colliculus neurons. Front. Integr. Neurosci. 4:6. doi: 10.3389/fnint.2010.00006
Davies, P. L., Chang, W. P., and Gavin, W. J. (2009). Maturation of sensory gating performance in children with and without sensory processing disorders. Int. J. Psychophysiol. 72, 187–197. doi: 10.1016/j.ijpsycho.2008.12.007
Davies, P. L., Chang, W. P., and Gavin, W. J. (2010). Middle and late latency ERP components discriminate between adults, typical children, and children with sensory processing disorders. Front. Integr. Neurosci. 4, 1–9. doi: 10.3389/fnint.2010.00016
Davies, P. L., and Gavin, W. J. (2007). Validating the diagnosis of sensory processing disorders using EEG technology. Am. J. Occup. Ther. 61, 176–189. doi: 10.5014/ajot.61.2.176
Davis, T. N., Lancaster, H. S., and Camarata, S. (2015). Expressive and receptive vocabulary learning in children with diverse disability typologies. Int. J. Dev. Disabil. 62:2047387715Y. doi: 10.1179/2047387715Y.0000000010
Demopoulos, C., Yu, N., Tripp, J., Mota, N., Brandes-Aitken, A. N., Desai, S. S., et al. (2017). Magnetoencephalographic imaging of auditory and somatosensory cortical responses in children with autism and sensory processing dysfunction. Front. Hum. Neurosci. 11:259. doi: 10.3389/fnhum.2017.00259
Diane Parham, L., Ecker, C., Kuhaneck, H. M., Henry, D. A., and Glennon, T. J. (2007). Sensory Processing Measure. Torrance: Western Psychological Services.
Eeles, A. L., Spittle, A. J., Anderson, P. J., Brown, N., Lee, K. J., Boyd, R. N., et al. (2013). Assessments of sensory processing in infants: a systematic review. Dev. Med. Child Neurol. 55, 314–326. doi: 10.1111/j.1469-8749.2012.04434.x
Fuentes-Santamaria, V., Alvarado, J. C., McHaffie, J. G., and Stein, B. E. (2009). Axon morphologies and convergence patterns of projections from different sensory-specific cortices of the anterior ectosylvian sulcus onto multisensory neurons in the cat superior colliculus. Cereb. Cortex. 19, 2902–2915. doi: 10.1093/cercor/bhp060
Fuentes-Santamaria, V., Alvarado, J. C., Stein, B. E., and McHaffie, J. G. (2008). Cortex contacts both output neurons and nitrergic interneurons in the superior colliculus: direct and indirect routes for multisensory integration. Cereb. Cortex. 18, 1640–1652. doi: 10.1093/cercor/bhm192
Gavin, W. J., Dotseth, A., Roush, K. K., Smith, C. A., Spain, H. D., and Davies, P. L. (2011). Electroencephalography in children with and without sensory processing disorders during auditory perception. Am. J. Occup. Ther. 65, 370–377. doi: 10.5014/ajot.2011.002055
Keuler, M. M., Schmidt, N. L., Van Hulle, C. A., Lemery-Chalfant, K., and Hill Goldsmith, H. (2011). Sensory overresponsivity: prenatal risk factors and temperamental contributions. J. Dev. Behav. Pediatr. 32, 533–541. doi: 10.1097/DBP.0b013e3182245c05
Kilroy, E., Aziz-Zadeh, L., and Cermak, S. (2019). Ayres theories of autism and sensory integration revisited: what contemporary neuroscience has to say. Brain Sci. 9:68. doi: 10.3390/brainsci9030068
Kuhn, T. (1970). The Structure of Scientific Revolutions. New York, NY: University of Chicago Press.
Lagasse, A. B., Manning, R., Crasta, J. E., Gavin, W. J., and Davies, P. L. (2019). Assessing the impact of music therapy on sensory gating and attention in children with autism: a pilot and feasibility study. J. Music Ther. 56, 287–314. doi: 10.1093/jmt/thz008
Lane, S. J., Miller, L. J., and Hanft, B. E. (2000). Toward a consensus in terminology in sensory integration theory and practice. Part 2, sensory integration patterns of function and dysfunction. Sens Integr. Spec. Interes. Sect. Quart. 23, 1–3. Available online at: http://sinetwork.org/wp-content/uploads/2017/06/TowardaConcensus-Part2.pdf
Larrauri, J. A., Burke, D. A., Hall, B. J., and Levin, E. D. (2015). Role of nicotinic receptors in the lateral habenula in the attenuation of amphetamine-induced prepulse inhibition deficits of the acoustic startle response in rats. Psychopharmacology 232, 3009–17. doi: 10.1007/s00213-015-3940-z
Larrauri, J. A., and Levin, E. D. (2012). The α2-adrenergic antagonist idazoxan counteracts prepulse inhibition deficits caused by amphetamine or dizocilpine in rats. Psychopharmacology 219, 2199–108. doi: 10.1007/s00213-011-2377-2
Levin, E. D., Caldwell, D. P., and Perraut, C. (2007). Clozapine treatment reverses dizocilpine-induced deficits of pre-pulse inhibition of tactile startle response. Pharmacol. Biochem. Behav. 86, 597–605. doi: 10.1016/j.pbb.2007.02.005
Levin, E. D., Petro, A., and Caldwell, D. P. (2005). Nicotine and clozapine actions on pre-pulse inhibition deficits caused by N-methyl-D-aspartate (NMDA) glutamatergic receptor blockade. Prog. Neuro-Psychopharmacol. Biol. Psychiatry. 29, 581–586. doi: 10.1016/j.pnpbp.2005.01.012
Mahendra, A., Skefos, J., Ghulam, M., Levin, E., and Bauman, M. (2012). A rat model of sensory integration impairment for therapeutic drug development: autoradiographic observations in postmortem brain. Available online at: https://insar.confex.com/insar/2012/webprogram/Paper11251.html
Marco, E. J., Aitken, A. B., Nair, V. P., Da Gente, G., Gerdes, M. R., Bologlu, L., et al. (2018). Burden of de novo mutations and inherited rare single nucleotide variants in children with sensory processing dysfunction. BMC Med. Genom. 11:50. doi: 10.1186/s12920-018-0362-x
Marco, E. J., Hinkley, L., Hill, S. S., and Nagarajan, S. S. (2011). Sensory processing in autism: a review of neurophysiologic findings. Pediatr. Res. 69, 48–54. doi: 10.1203/PDR.0b013e3182130c54
Marco, E. J., Khatibi, K., Hill, S. S., Siegel, B., Arroyo, M. S., Dowling, A. F., et al. (2012). Children with autism show reduced somatosensory response: an MEG study. Autism Res. 5, 340–351. doi: 10.1002/aur.1247
McIntosh, D. N., Miller, L. J., Shyu, V., and Hagerman, R. J. (1999). Sensory-modulation disruption, electrodermal responses, and functional behaviors. Dev. Med. Child Neurol. 41, 608–615. doi: 10.1017/S0012162299001267
Miller, L. J., Anzalone, M. E., Lane, S. J., Cermak, S. A., and Osten, E. T. (2007a). Concept evolution in sensory integration: a proposed nosology for diagnosis. Am. J. Occup. Ther. 61, 135–40. doi: 10.5014/ajot.61.2.135
Miller, L. J., Chu, R. C., Parkins, M., Spielmann, V. A., and Schoen, S. A. (2020b). “The STAR PROCESS: an overview,” in: Sensory Integration: Theory and Practice, 3 edn, eds A. C. Bundy, S. J. Lane (Philadelphia, PA: F. A. Davis Company), 578–85.
Miller, L. J., Coll, J. R., and Schoen, S. A. (2007b). A randomized controlled pilot study of the effectiveness of occupational therapy for children with sensory modulation disorder. Am. J. Occup. Ther. 61, 228–38. doi: 10.5014/ajot.61.2.228
Miller, L. J., and Lane, S. J. (2000). Toward a consensus in terminology in sensory integration theory and practice: Part 1: taxonomy of neurophysiological processes. Sens. Integr. Spec. Interes. Sect. Quart. 23, 1–4. Available online at: http://sinetwork.org/wp-content/uploads/2017/06/TowardaConcensus-Part2.pdf
Miller, L. J., McIntosh, D. N., McGrath, J., Shyu, V., Lampe, M., Taylor, A. K., et al. (1999). Electrodermal responses to sensory stimuli in individuals with fragile X syndrome: a preliminary report. Am. J. Med. Genet. 83, 268–279. doi: 10.1002/(SICI)1096-8628(19990402)83:4<268::AID-AJMG7>3.0.CO;2-K
Miller, L. J., Nielsen, D. M., Schoen, S. A., and Brett-Green, B. A. (2009). Perspectives on sensory processing disorder: a call for translational research. Front. Integr. Neurosci. 3:22. doi: 10.3389/neuro.07.022.2009
Miller, L. J., Reisman, J. E., McIntosh, D. N., and Simon, J. (2001). “An ecological model of sensory modulation: performance of children with fragile X syndrome, autistic disorder, attention-deficit/hyperactivity disorder, and sensory modulation dysfunction,” in: Understanding the Nature of Sensory Integration With Diverse Populations, eds S. S. Roley, E. I. Blanche, R. C. Schaaf (Austin, TX: Pro-Ed), 57–88.
Miller, L. J., Schoen, S. A., and Mulligan, S. (2020a). The Sensory Processing Three Dimensions Scale (SP3D: Research Edition). Torrance: Western Psychological Services.
Miller, L. J., Schoen, S. A., and Spielmann, V. A. (2018). “A frame of reference for sensory processing difficulties: sensory therapies and research (STAR),” in:. Frames of Reference for Pediatric Occupational Therapy, 4th edn, eds P. Kramer, J. Hinojosa, T. Howe (Philadelphia, PA: Wolters Kluwer), 159–202.
Miller, R. L., Stein, B. E., and Rowland, B. A. (2017). Multisensory integration uses a real-time unisensory–multisensory transform. J. Neurosci. 37, 5183–5194. doi: 10.1523/JNEUROSCI.2767-16.2017
Moore, C. F., Gajewski, L. L., Laughlin, N. K., Luck, M. L., Larson, J. A., and Schneider, M. L. (2008). Developmental lead exposure induces tactile defensiveness in rhesus monkeys (Macaca Mulatta). Environ. Health Perspect. 116, 1322–6. doi: 10.1289/ehp.11203
Mukherjee, P., Chang, Y. S., Owen, J. P., Desai, S. S., Hill, S. S., Arnett, A. B., et al. (2014). Autism and sensory processing disorders: shared white matter disruption in sensory pathways but divergent connectivity in social-emotional pathways. PLoS ONE 9:e103038. doi: 10.1371/journal.pone.0103038
Mulligan, S., Schoen, S., Miller, L., Valdez, A., Wiggins, A., Hartford, B., et al. (2019b). Initial studies of validity of the sensory processing 3-dimensions scale. Phys. Occup. Ther. Pediatr. 39, 94–106. doi: 10.1080/01942638.2018.1434717
Mulligan, S., Schoen, S. A., Miller, L. J., Valdez, A., and Magalhaes, D. (2019a). The sensory processing 3-dimensions scale: initial studies of reliability and item analyses. Open J. Occup. Ther. 7:71–12. doi: 10.15453/2168-6408.1505
Owen, J. P., Marco, E. J., Desai, S., Fourie, E., Harris, J., Hill, S. S., et al. (2013). Abnormal white matter microstructure in children with sensory processing disorders. NeuroImage Clin. 2, 844–853. doi: 10.1016/j.nicl.2013.06.009
Payabvash, S., Palacios, E. M., Owen, J. P., Wang, M. B., Tavassoli, T., Gerdes, M., et al. (2019). Diffusion tensor tractography in children with sensory processing disorder: potentials for devising machine learning classifiers. NeuroImage Clin. 23:101831. doi: 10.1016/j.nicl.2019.101831
Pennington, B. (1991). “Issues in syndrome validation,” in: Diagnosing Learning Disorders, eds L. M. McGrath and R. L. Peterson (New York, NY: The Guilford Press), 23–31.
Pfeiffer, B. A., Koenig, K., Kinnealey, M., Sheppard, M., and Henderson, L. (2011). Effectiveness of sensory integration interventions in children with autism spectrum disorders: a pilot study. Am. J. Occup. Ther. 65, 76–85. doi: 10.5014/ajot.2011.09205
Roegge, C. S., Perraut, C., Hao, X., and Levin, E. D. (2007). Histamine H1 receptor involvement in prepulse inhibition and memory function: relevance for the antipsychotic actions of clozapine. Pharmacol. Biochem. Behav. 86, 686–692. doi: 10.1016/j.pbb.2007.02.014
Rowland, B. A., Jiang, W., and Stein, B. E. (2014). Brief cortical deactivation early in life has long-lasting effects on multisensory behavior. J. Neurosci. 34, 7198–7202. doi: 10.1523/JNEUROSCI.3782-13.2014
Schaaf, R. C., Benevides, T., Mailloux, Z., Faller, P., Hunt, J., Van Hooydonk, E., et al. (2014). An intervention for sensory difficulties in children with autism: a randomized trial. J. Autism Dev. Disord. 44, 1493–1506. doi: 10.1007/s10803-014-2111-0
Schmajuk, N. A., Larrauri, J. A., De la Casa, L. G., and Levin, E. D. (2009). Attenuation of auditory startle and prepulse inhibition by unexpected changes in ambient illumination through dopaminergic mechanisms. Behav. Brain Res. 197, 251–261. doi: 10.1016/j.bbr.2008.08.030
Schmajuk, N. A., Larrauri, J. A., Hagenbuch, N., Levin, E. D., Feldon, J., and Yee, B. K. (2006). Startle and prepulse inhibition as a function of background noise: a computational and experimental analysis. Behav. Brain Res. 170, 182–196. doi: 10.1016/j.bbr.2006.02.021
Schneider, M. L., Kraemer, G. W., and Suomi, S. J. (1991). The effects of vestibular-proprioceptive stimulation on motor maturation and response to challenge in rhesus monkey infants. Occup. Ther. J. Res. 11, 135–154. doi: 10.1177/153944929101100302
Schneider, M. L., Larson, J. A., Rypstat, C. W., Resch, L. M., Roberts, A., and Moore, C. F. (2013). Moderate-level prenatal alcohol exposure enhances acoustic startle magnitude and disrupts prepulse inhibition in adult rhesus monkeys. Alcohol. Clin. Exp. Res. 37, 1729–1736. doi: 10.1111/acer.12151
Schneider, M. L., Moore, C. F., Adkins, M., Barr, C. S., Larson, J. A., Resch, L. M., et al. (2017). Sensory processing in rhesus monkeys: developmental continuity, prenatal treatment, and genetic influences. Child Dev. 88, 183–197. doi: 10.1111/cdev.12572
Schneider, M. L., Moore, C. F., and Adkins, M. M. (2011). The effects of prenatal alcohol exposure on behavior: rodent and primate studies. Neuropsychol. Rev. 21, 186–203. doi: 10.1007/s11065-011-9168-8
Schneider, M. L., Moore, C. F., Gajewski, L. L., Larson, J. A., Roberts, A. D., Converse, A. K., et al. (2008). Sensory processing disorder in a primate model: evidence from a longitudinal study of prenatal alcohol and prenatal stress effects. Child Dev. 79, 100–113. doi: 10.1111/j.1467-8624.2007.01113.x
Schneider, M. L., Moore, C. F., Gajewski, L. L., Laughlin, N. K., Larson, J. A., Gay, C. L., et al. (2007). Sensory processing disorders in a non-human primate model: evidence for occupational therapy practice. Am. J. Occup. Ther. 61, 247–253. doi: 10.5014/ajot.61.2.247
Schneider, M. L., Moore, C. F., Larson, J. A., Barr, C. S., DeJesus, O. T., and Roberts, A. D. (2009). Timing of moderate level prenatal alcohol exposure influences gene expression of sensory processing behavior in rhesus monkeys. Front. Integr. Neurosci. 3:30. doi: 10.3389/neuro.07.030.2009
Schoen, S. A., Miller, L. J., Brett-Green, B. A., and Nielsen, D. M. (2009). Physiological and behavioral differences in sensory processing: a comparison of children with autism spectrum disorder and sensory modulation disorder. Front. Integr. Neurosci. 3:29. doi: 10.3389/neuro.07.029.2009
Schoen, S. A., Miller, L. J., Camarata, S., and Valdez, A. (2019). Use of the STAR PROCESS for children with sensory processing challenges. Open J. Occup. Ther. 7, 1–17. doi: 10.15453/2168-6408.1596
Schoen, S. A., Miller, L. J., and Flanagan, J. (2018). A retrospective pre-post treatment study of occupational therapy intervention for children with sensory processing challenges. Open J. Occup. Ther. 6, 1–14. doi: 10.15453/2168-6408.1367
Schoen, S. A., Miller, L. J., and Green, K. E. (2008). Pilot study of the sensory over-responsivity scales: assessment and inventory. Am. J. Occup. Ther. 62, 393–406. doi: 10.5014/ajot.62.4.393
Schoen, S. A., Miller, L. J., and Nielsen, D. M. (2014a). “Sensory integrative theory and treatment: occupational therapy with a sensory integrative approach,” in Autism Interventions: Exploring the Spectrum of Autism, eds C. Murray-Slutsky, and B. Paris (Austin, TX: Hammill Institute on Disabilities), 27–51.
Schoen, S. A., Miller, L. J., and Sullivan, J. (2017). The development and psychometric properties of the Sensory Processing Scale Inventory: a report measure of sensory modulation. J. Intellect. Dev. Disabil. 42, 12–21. doi: 10.3109/13668250.2016.1195490
Schoen, S. A., Miller, L. J., and Sullivan, J. C. (2014b). Measurement in sensory modulation: the sensory processing scale assessment. Am. J. Occup. Ther. 68, 522–530. doi: 10.5014/ajot.2014.012377
Skefos, J., Ghulam, M., Mahendra, A., Patel, G., Larrauri, J., Kholdebarin, E., et al. (2014). Histamine and acetylcholine receptor involvement in sensorimotor gating: an autoradiography study. F1000Research 3:136. doi: 10.12688/f1000research.4287.1
Skuse, D. H. (2000). Behavioural phenotypes: what do they teach us? Arch. Dis. Child. 82, 222–225. doi: 10.1136/adc.82.3.222
Stein, B. E. (1998). Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Exp. Brain Res. 123, 124–35. doi: 10.1007/s002210050553
Stein, B. E., Stanford, T. R., and Rowland, B. A. (2009). The neural basis of multisensory integration in the midbrain: its organization and maturation. Hear. Res. 258, 4–15. doi: 10.1016/j.heares.2009.03.012
Stevenson, R. A., Segers, M., Ferber, S., Barense, M. D., Camarata, S., and Wallace, M. T. (2016). Keeping time in the brain: autism spectrum disorder and audiovisual temporal processing. Autism Res. 9, 720–738. doi: 10.1002/aur.1566
Stevenson, R. A., Siemann, J. K., Schneider, B. C., Eberly, H. E., Woynaroski, T. G., Camarata, S. M., et al. (2014a). Multisensory temporal integration in autism spectrum disorders. J. Neurosci. 34, 691–697. doi: 10.1523/JNEUROSCI.3615-13.2014
Stevenson, R. A., Siemann, J. K., Woynaroski, T. G., Schneider, B. C., Eberly, H. E., Camarata, S. M., et al. (2014b). Brief report: arrested development of audiovisual speech perception in autism spectrum disorders. J. Autism Dev. Disord. 44, 1470–1477. doi: 10.1007/s10803-013-1992-7
Stevenson, R. A., Siemann, J. K., Woynaroski, T. G., Schneider, B. C., Eberly, H. E., Camarata, S. M., et al. (2014c). Evidence for diminished multisensory integration in autism spectrum disorders. J. Autism Dev. Disord. 44, 3161–3167. doi: 10.1007/s10803-014-2179-6
Tavassoli, T., Brandes-Aitken, A., Chu, R., Porter, L., Schoen, S., Miller, L. J., et al. (2019). Sensory over-responsivity: parent report, direct assessment measures, and neural architecture. Mol. Autism. 10:4. doi: 10.1186/s13229-019-0255-7
Tavassoli, T., Miller, L. J., Schoen, S. A., Jo Brout, J., Sullivan, J., and Baron-Cohen, S. (2018). Sensory reactivity, empathizing and systemizing in autism spectrum conditions and sensory processing disorder. Dev. Cogn. Neurosci. 29, 72–77. doi: 10.1016/j.dcn.2017.05.005
Tavassoli, T., Miller, L. J., Schoen, S. A., Nielsen, D. M., and Baron-Cohen, S. (2014). Sensory over-responsivity in adults with autism spectrum conditions. Autism 18, 428–432. doi: 10.1177/1362361313477246
Van Hulle, C., Lemery-Chalfant, K., and Hill Goldsmith, H. (2015). Trajectories of sensory over-responsivity from early to middle childhood: birth and temperament risk factors. PLoS ONE 10:e0129968. doi: 10.1371/journal.pone.0129968
Van Hulle, C. A., Esbensen, K., and Hill Goldsmith, H. (2019). Co-occurrence of sensory overresponsivity with obsessive-compulsive symptoms in childhood and early adolescence. J. Dev. Behav. Pediatr. 40, 377–382. doi: 10.1097/DBP.0000000000000671
Van Hulle, C. A., Lemery-Chalfant, K., and Hill Goldsmith, H. (2018). Parent-offspring transmission of internalizing and sensory over-responsivity symptoms in adolescence. J. Abnorm. Child Psychol. 46, 557–567. doi: 10.1007/s10802-017-0300-y
Van Hulle, C. A., Schmidt, N. L., and Hill Goldsmith, H. (2012). Is sensory over-responsivity distinguishable from childhood behavior problems? A phenotypic and genetic analysis. J. Child Psychol. Psychiatry Allied Discip. 53, 64–72. doi: 10.1111/j.1469-7610.2011.02432.x
Wickremasinghe, A. C., Rogers, E. E., Johnson, B. C., Shen, A., Barkovich, A. J., and Marco, E. J. (2013). Children born prematurely have atypical sensory profiles. J. Perinatol. 33, 631–635. doi: 10.1038/jp.2013.12
Xu, J., Yu, L., Stanford, T. R., Rowland, B. A., and Stein, B. E. (2015). What does a neuron learn from multisensory experience? J. Neurophysiol. 113, 883–889. doi: 10.1152/jn.00284.2014
Yeung, L. H. J., and Thomacos, N. (2020). Assessments of sensory processing in infants and children with autism spectrum disorder between 0 and 12 years old: a scoping review. Res. Autism Spectr. Disord. 72:101517. doi: 10.1016/j.rasd.2020.101517
Yu, L., Rowland, B. A., and Stein, B. E. (2010). Initiating the development of multisensory integration by manipulating sensory experience. J. Neurosci. 30, 4904–4913. doi: 10.1523/JNEUROSCI.5575-09.2010
Yu, L., Stein, B. E., and Rowland, B. A. (2009). Adult plasticity in multisensory neurons: short-term experience-dependent changes in the superior colliculus. J. Neurosci. 29, 15910–15922. doi: 10.1523/JNEUROSCI.4041-09.2009
Keywords: sensory processing, sensory integration, neurophysiology of sensation, sensory phenotype, treatment effectiveness
Citation: Miller LJ, Marco EJ, Chu RC and Camarata S (2021) Editorial: Sensory Processing Across the Lifespan: A 25-Year Initiative to Understand Neurophysiology, Behaviors, and Treatment Effectiveness for Sensory Processing. Front. Integr. Neurosci. 15:652218. doi: 10.3389/fnint.2021.652218
Received: 12 January 2021; Accepted: 24 February 2021;
Published: 09 April 2021.
Edited and reviewed by: Elizabeth B. Torres, Rutgers, The State University of New Jersey, United States
Copyright © 2021 Miller, Marco, Chu and Camarata. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Lucy Jane Miller, bHVjeW1pbGxlcnBoZCYjeDAwMDQwO2dtYWlsLmNvbQ==
†ORCID: Stephen Camarata orcid.org/0000-0002-3342-1747