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Sensory Phenotypes in Autism: Making A Case For The Inclusion of Sensory Integration Functions

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Journal of Autism and Developmental Disorders

https://doi.org/10.1007/s10803-022-05763-0

S:I: .DEVELOPMENTAL APPROACH AND


TARGETED TREATMENT OF SENSORY

Sensory Phenotypes in Autism: Making a Case for the Inclusion of


Sensory Integration Functions
Roseann C. Schaaf1  · Zoe Mailloux1 · Elizabeth Ridgway2 · Alaina S. Berruti3 · Rachel L. Dumont1 · Emily A. Jones4 ·
Benjamin E. Leiby5 · Catherine Sancimino3 · Misung Yi5 · Sophie Molholm6

Accepted: 14 September 2022


© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2022

Abstract
Sensory features are part of the diagnostic criteria for autism and include sensory hypo/hyper reactivity and unusual
sensory interest; however, additional sensory differences, namely differences in sensory integration, have not been rou-
tinely explored. This study characterized sensory integration differences in a cohort of children (n = 93) with a confirmed
diagnosis of autism (5–9 years) using a standardized, norm-referenced battery. Mean z scores, autism diagnostic scores,
and IQ are reported. Participants showed substantial deficits in tactile perception, praxis, balance, visual perception, and
visual-motor skills. Relationship with autism diagnostic test scores were weak or absent. Findings suggest additional
sensory difficulties that are not typically assessed or considered when characterizing sensory features in autism. These
data have implications for a greater understanding of the sensory features in the autism phenotype and the development
of personalized treatments.

Keywords  Autism · Sensation · Perception · Symptom Assessment

Atypical sensory behaviors are a part of the DSM5 diagnos- Profile 2 (Dunn, 2014), the Sensory Processing Measure 2
tic criteria for autism spectrum disorder (ASD) (APA, 2013) (Parham et al., 2007), or the Sensory Experiences Question-
and include hypo and/or hyper-reactivity to sensation (here- naire (Baranek et al., 2006). These assessments, while valu-
after referred to as sensory reactivity) and unusual interests in able, are not intended to capture many important aspects of
the sensory aspects of the environment. Currently, these are sensory perceptual and sensorimotor skills in ASD reported
assessed using parent-report measures such as the Sensory in the literature (Robertson & Baron-Cohen, 2015), such as
sensory perception (the detection, discrimination, character-
izing, and recognizing sensory information), multisensory
Roseann C. Schaaf integration (the process by which inputs from two or more
Roseann.Schaaf@jefferson.edu senses are combined to influence perception and behavior
1
(Stein, et al., 2014; Molholm, 2002), praxis (the use of sen-
Jefferson Autism Center of Excellence, Department of
Occupational Therapy, Thomas Jefferson University College sory information to plan and execute goal-directed tasks
of Rehabilitation Sciences, Philadelphia, PA, USA (Ayres, 1989; Mostofsky, 2011), and other sensorimotor
2
Department of Pediatrics, Rose F. Kennedy Children’s functions (such as balance, bilateral motor coordination,
Evaluation and Rehabilitation Center, Albert Einstein College and visual motor skills) (Hannant et al., 2016). Collectively,
of Medicine, Montefiore, Bronx, NY, USA these functions are referred to as ‘sensory integration,‘ or
3
The Cognitive Neurophysiology Laboratory, Department of the “integration of sensation for use” (Ayres, 1972, 1979).
Pediatrics, Albert Einstein College of Medicine, Research shows that challenges in sensory integration are
10461 Bronx, NY, USA prevalent in autistic persons and impact functional skills
4
Queens College and the Graduate Center, City University of and abilities such as the ability to act and interact in daily
New York, Queens, NY, USA life (Smith-Roley et al., 2015; Williams et al., 2018; Trav-
5
Division of Biostatistics, Thomas Jefferson University, ers et al.,2022; Schaaf, et al., 2011; Brandwein, et al., 2013,
Philadelphia, PA, USA Crosse, et al., 2019; Crosse, et al., in press). Thus, the sen-
6
Department of Neuroscience, Albert Einstein College of sory differences experienced by autistic persons go beyond
Medicine, 10461 Bronx, NY, USA

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Journal of Autism and Developmental Disorders

sensory reactivity and sensory seeking to include additional integration treatment. Ethics approval was obtained from
types and characteristics. A comprehensive assessment of the institutional review board at the Albert Einstein College
these functions is necessary to fully appreciate the extent of Medicine. A licensed clinical psychologist with research
and nature of sensory integrative challenges in autistic per- reliability and extensive experience in the diagnosis of ASD
sons. These comprehensive assessment data may further made or confirmed a diagnosis of ASD based on the Autism
inform the sensory features in the autism phenotype and Diagnostic Observation Schedule, 2nd Edition (ADOS-2;
guide individualized interventions. Lord et al., 2012), developmental history, and clinical judg-
While there is a preponderance of literature character- ment; and measured IQ using the Wechsler Abbreviated
izing types, subtypes, and patterns of sensory reactivity Scale of Intelligence, Second Edition (WASI-II; Wechsler,
in autistic groups, there has been less exploration of these 2011). Inclusion criteria were a diagnosis of ASD between
other sensory integration functions and their impact on the ages of 6 and 9.5 years at the onset of the study, a non-
function and participation in individuals with ASD. Fur- verbal IQ score greater than 65, and evidence of sensory dys-
ther, most characterizations of sensory functions in ASD function as measured by the Sensory Integration and Praxis
are based on parent or caregiver reports of behaviors that Tests (SIPT; Ayres, 1989) and/or the Sensory Processing
are hypothesized to directly link to sensory disturbances Measure (Parham, 2007). Children with limitations in their
rather than a performance-based assessment. Best-practices ability to engage in active, sensory-motor activities (i.e.,
in assessment of sensory features recommend a combina- physical limitations), a genetic syndrome, hearing impair-
tion of proxy reports and observational/performance-based ment, or uncorrected visual impairment were excluded from
assessments to obtain a comprehensive picture of sensory the study. Participant demographics, including age, gen-
differences and their impact on function, performance, der, race, and ethnicity are shown in Table  1. In addition,
and participation (Schaaf and Lane, 2015). Hence, there is autism severity scores from the ADOS-2 and IQ scores are
a need to objectively and systematically characterize sen- shown. As expected, there was a greater number of males
sory integrative differences in ASD to specify their extent than females. Full scale IQ scores ranged from 50 to 166
and nature clearly. In addition, assessment data about the (mean = 87.6; SD = 20.5) while non-verbal or performance
sensory integrative factors that may be impacting autistic IQ (PIQ) ranged from 56 to 143 (mean = 93.7, SD = 18.5)
person’s function and participation can be helpful for tai- and autism severity ranged from low to high.
loring or individualizing interventions designed to improve
sensory and sensorimotor factors that impact participation
in activities and tasks. The purpose of this paper is to fur- Procedures
ther characterize sensory differences in ASD by exploring
sensory integration functions. To this end, results from the The procedures for the collection of intake data for the ran-
Sensory Integration and Praxis Tests (SIPT; Ayres, 1989) domized controlled trial that these data are associated with
are reported in a cohort of children with ASD. The SIPT is these data are described in more detail in a recent publica-
a set of performance-based, standardized, and normed psy- tion (Beker, et al., 2021). All assessments were completed
chometric tests designed to assess function in multiple areas by research-certified examiners with advanced training.
of sensory integration.

Instruments
Methods
The Sensory Integration and Praxis Tests (SIPT)
Design
The SIPT consists of 17 tests, standardized on 1,997 chil-
This study utilized a descriptive, cross-sectional analysis of dren ages 4 yrs. to 8 yrs., 11 mo., designed to assess visual,
pre-treatment scores on the ADOS-2 and the Sensory Inte- tactile, vestibular and proprioceptive perception, visual–
grative and Praxis Tests. motor skills, praxis, balance, and bilateral integration
(Ayres, 1989). The SIPT is used mainly within occupational
therapy to test distinct and varied sensory integrative func-
Participants tions. The tests and the function(s) that each test is designed
to assess are shown in Table  2. For the current study, the
The sample reported in this study is from a larger ran- SIPT was administered by an occupational therapist with
domized controlled trial of children with ASD who were advanced training in its administration and interpretation.
enrolled in a comparative effectiveness trial of sensory The total test time for the SIPT is about 2–3 h, depending on

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Journal of Autism and Developmental Disorders

Table 1
Demographic Characteristics
N N miss Mean SD Min Max
ADOS2 SA Total (calibrated) 93 0 7.48 1.82 1.00 10.00
ADOS2 RRB Total (calibrated) 93 0 8.62 1.37 4.00 10.00
ADOS2 D-1 93 0 1.38 0.90 0.00 3.00
ADOS2 Severity Score/Comparison Score 93 0 8.08 1.58 5.00 10.00
Age 93 0 7.06 1.08 5.00 9.00
VIQ 93 0 80.67 22.54 45.00 130.0
PIQ 93 0 93.66 18.47 56.00 143.0
FSIQ 93 0 87.61 20.52 50.00 166.0
Gender N %
Male 80 86.02%
Female 13 13.98%
Race N %
White 24 25.81
Black or African American 24 25.81
Asian 8 8.60
Hawaiian or Pacific Islander 2 2.15
Multiple Races 17 18.28
Unknown or refused to answer 12 12.90
Ethnicity N %
Hispanic or Latino 51 54.84
Non-Hispanic or Latino 29 31.18
Missing 10 10.75
Unknown or refused to answer 3 3.23
Age
5 2 2.15%
6 35 37.63%
7 21 22.58%
8 25 26.88%
9 10 10.75%
ADOS D-1
0 18 19.35%
1 30 32.26%
2 37 39.78%
3 8 8.60%
Some children did not complete portions of the ADOS testing and thus, total n may vary. ADOS2 = Autism Diagnostic Observation Scale Sec-
ond Edition; SA = Social Affect; RRB = Restrictive, Repetitive Behaviors, D-1 = Sensory Score. VIQ = verbal intelligence quotient; PIQ = per-
formance intelligence quotient; FSIQ = full scale intelligence quotient

the number of breaks needed. It can be administered in mul- based on age-normative data. On the SIPT, z scores ≤ -1.0
tiple sessions. Testers received advanced training in admin- indicate areas of concern. One exception is the Post Rotary
istration and scoring of SIPT prior to study initiation and Nystagmus (PRN) test, where a score of ≤ -1.0 or ≥ + 1.0
were evaluated for adherence to administration procedures are considered clinically meaningful (Ayres, 1989). Thus,
by the first author. Psychometric properties of the SIPT are the z score reflects each participant’s rating, with a score
strong (Ayres, 1989); each SIPT test has high interrater falling below − 1.0 indicating below age-expectancy per-
reliability (r = .94-0.99), discriminates between typical and formance. For the 10 participants who exceeded the age
atypical samples (p < .01 ;), and has content and construct norms, the oldest age norm for z scoring is referenced. This
validity (Ayres, 1989). produces a conservative assessment of atypicality of SIPT
Each test of the SIPT is administered using simple visual performance.
demonstration and standardized verbal instructions except
Praxis on Verbal Command, which is solely language
dependent and involves simple language instructions to the
child. SIPT yields raw scores that are converted to z scores

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Journal of Autism and Developmental Disorders

Table 2  Sensory Integration and Praxis Tests and Functions They and Repetitive Behaviors (RRB) were generated (Hus et al.,
Measure
2014).
Somatosensory Perception
The ADOS-2 scoring item D-1, Unusual Sensory Inter-
Manual Form Perception (MFP) Identification of shapes
placed in hand by touch est in Play Material/Person, is used to code all observa-
Finger Identification (FI) Identification of finger(s) tions of atypical sensory interests or behaviors (Lord et al.,
touched without vision 2012). D-1 falls within the RRB category of the ADOS-2
Graphesthesia (GRA) Replication of simple designs algorithm. Scores range from 0 to 3, with 0 indicating no
drawn on the dorsum of hand sensory-related behaviors observed and 3 indicating definite
Kinesthesia (KIN) FI + Gra + MFP
sensory behaviors observed. Examples of sensory behaviors
Praxis
leading to elevated scores on item D-1 include behaviors
Postural Praxis (PPr) Imitation of novel body and
hand postures such as the repetitive feeling of texture, strong interest in the
Oral Praxis (OPr) Imitation of mouth and facial repetition of certain sounds, and prolonged visual examina-
postures and actions tion (Lord et al., 2012).
Sequencing Praxis (SPr) Imitation of novel hand
sequential actions
Praxis on Verbal Command (PrVC) Ability to demonstrate novel
postures and actions based on
Cognitive Testing
simple verbal directions
Praxis Composite PPr, OPr, SPr, PrVC To determine eligibility for participation in this study, the
Vestibular and Proprioceptive Functions and Bilateral Motor cognitive ability of all participants was measured using the
Skills WASI-II; Wechsler, 2011). The WASI-II is a reliable mea-
Kinesthesia (KIN) Replication of arm position sure of general cognitive ability, yielding full-scale, verbal,
and movement
and performance index scores obtained by administering all
Standing and Walking Balance Static and dynamic balance
(SWB) four subtests (30–45 min) or two subtests (~ 15 min) of the
Postrotary Nystagmus (PRN) Vestibular-ocular reflex fol- WASI-II. The WASI-II is normed for ages 6–89 years and
lowing rotation is appropriate for use with individuals with a wide range of
Bilateral Motor Coordination Replication of bilateral arm abilities (index scores range from 40 to 160). A non-verbal
(BMC): and foot movements IQ of ≥ 65 was needed for inclusion in the study. We have
Vestibular-Proprioception Kin, SWB, BMC found that non-verbal IQ provides a good measure of ability
Composite
to engage in tasks such as those required for the assessments
Visual Perception and Visual Motor
Space Visualization (SV) Motor-free visual spatial
and treatment in this study.
perception
Figure Ground Perception (FG) Motor-free ability to find fig- Data Analysis
ures embedded in background
Motor Accuracy (MAc) Tracing over line with pencil Descriptive statistics for the z scores of each SIPT test
Design Copying (DC) Replication of designs by (group mean, SD, and % ≤ -1) are displayed in Table  3,
drawing
and a depiction of the distribution of the individual scores
Constructional Praxis (CPr) Replication of block structures
Visual Composite SV + FG + MAC + CPr as well as how they distribute as a function of IQ are dis-
played in Box Plots on Fig. 1. In addition to reporting on
mean z scores for each test, we created composite scores
Autism Diagnostic Observation Schedule, Second for sensory integrative functions. These four composite
Edition (ADOS-2) scores are based on prior factor analytic studies showing
that certain tests cluster on a single factor (Ayres, 1989;
Each participant was administered the ADOS-2, a semi- Mailloux et al., 2011; Mulligan, 1996). Composite scores
structured observational assessment developed for a trained were calculated by averaging all non-missing SIPT test
examiner to identify behaviors associated with ASD (Lord z-scores contributing to a particular composite score. These
et al., 2012). It is a reliable and valid instrument used to were used to examine whether ADOS Social Affect (SA)
assess individuals across different developmental levels and score, Restricted Repetitive Behaviors (RRB) score, and
chronological ages (Carr, 2013). Based on the age and lan- ADOS D-1 score and IQ scores were related to SIPT scores
guage level of research participants, ADOS-2 Module 1, 2, using correlational analyses. We used full-scale IQ for these
or 3 was administered. ADOS-2 severity scores and cali- analyses as it provides an overall representation of cogni-
brated domain scores for Social Affect (SA) and Restricted tive ability. A tactile perception composite score was gener-
ated from the mean score on three tactile perception tests:

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Journal of Autism and Developmental Disorders

Table 3  SIPT Tests Mean z Scores, Standard Deviations, Frequency and Percentages
Test Name and Description N Mean z SD Min Max Fre-
score quency/
percent
<-1.0
Tactile Perception
Manual Form Perception (MFP) 89 -1.76 1.43 -3.00 1.50 61/69
Finger Identification (FI) 83 -0.97 1.32 -3.00 1.62 38/46
Graphesthesia (GRA) 77 -1.77 1.05 -3.00 0.81 60/78
Tactile Perception Composite 90 -1.58 1.02 -3.00 1.20 60/67
Praxis
Postural Praxis (PPr) 91 -2.37 0.89 -3.00 1.01 84/92
Oral Praxis (OPr) 90 -2.20 0.93 -3.00 1.24 79/88
Sequencing Praxis (SPr) 90 -1.57 1.25 -3.00 2.82 62/69
Praxis on Verbal Command (PrVC) 90 -2.35 1.06 -3.00 0.46 77/86
Praxis Composite 92 -2.14 0.76 -3.00 -0.07 85/92
Vestibular and Proprioceptive Functions and Bilateral Motor Skills
Kinesthesia (KIN) 69 -1.42 1.21 -3.00 1.33 41/59
Standing Walking Balance (SWB) 92 -2.64 0.64 -3.00 -0.54 89/97
Bilateral Motor Coordination (BMC) 91 -1.04 1.02 -3.00 1.36 52/57
Composite: Kin, SWB, BMC 92 -1.78 0.70 -3.00 0.08 80/87
Visual Perception and Visual Motor
Space Visualization (SV) 92 -1.25 1.03 -3.00 0.79 54/59
Figure Ground Perception (FG) 93 -1.07 1.06 -3.00 2.45 53/57
Motor Accuracy (MAC) 91 -0.84 1.36 -3.00 2.06 43/47
Design Copying (DC) 90 -1.38 1.49 -3.00 2.15 55/61
Constructional Praxis (CPr) 90 -1.07 1.30 -3.00 1.60 47/52
Visual Composite 93 -1.07 0.84 -2.79 0.99 50/54
SD = standard deviation, min = lowest score; max = highest score; percent = percent of sample
Postrotary Nystagmus (PRN): scores were not included in Vestibular and Proprioceptive Functions and Bilateral Motor Skills composite
because scores below − 1.0 and above + 1.0 are indicative of dysfunction. PRN below − 1.0 (n = 24; 29%); PRN above + 1.0 (n = 20; 24%).

Manual Form Perception (MFP), Finger Identification (FI), from the composite score because both high and low scores
and Graphesthesia (GRA). Therefore, the composite mean are reflective of dysfunction, thus negating the use of mean
score consists of the MFP, FI, and GRA mean score based score analyses (Ayres, 1989). A visual perception and visual
on all participants who completed this test. An additional motor composite score was generated from two motor-free
tactile perception test that is part of the SIPT, Localization tests of visual perception (Space Visualization; SV) and Fig-
of Tactile Stimuli, was omitted because this test often shows ure Ground (FG), two tests of visual motor skills (Motor
high scores in children with tactile hyper-reactivity (Ayres, Accuracy; MAC) and Design Copy (DC)), and one test of
1989) and thus, may not be a reliable reflection of tactile block design replication (Constructional Praxis (CPr). We
perception in autistic children, many of whom experience included CPr within this composite because it utilizes visual
tactile hyper-reactivity. perception and visual motor skills, and in prior studies,
Similarly, a praxis composite score was generated from it correlated highly with the other tests in this composite
three tests of imitation praxis (Postural Praxis (PPr), Oral group (Ayres, 1989; Van Jaarsveld et al., 2014).
Praxis (OPr), and Sequencing Praxis (SPr)) and one test of
praxis from verbal directions (Praxis on Verbal Command-
PrVC). The vestibular-proprioceptive and bilateral motor Results
skills composite score was generated from one test of pro-
prioception (Kinesthesia; KIN), one test of balance (Stand- ADOS-2 Scores
ing and Walking Balance; SWB), and one test of bilateral
motor coordination (BMC). Both balance and bilateral coor- As shown in Table 1, the ADOS-2 SA scores ranged from
dination have been consistently associated with vestibular- 4 to 10, with a mean score of 7.5 (1.83). Of note, only one
proprioceptive functions on factor analytic studies (Ayres, participant obtained an SA total score of 4, and this indi-
1989; Mailloux et al., 2011; Mulligan, 1996). A test of ves- vidual met diagnostic criteria for ASD. ADOS-2 RRB
tibular function, the Postrotary Nystagmus test, was omitted scores ranged from 4 to 10, with a mean score of 8.7 (1.35).

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Journal of Autism and Developmental Disorders

Fig. 1  Boxplots for SIPT and


ADOS Legend: Dark line
represents median; star repre-
sents mean. MFP = Manual Form
Perception Test, FI = Finger Iden-
tification Test, GRA = Graphes-
thesia Test, KIN = Kinesthe-
sia Test, SWB = Standing
and Walking Balance Test,
BMC = Bilateral Motor Coordina-
tion Test; PPr = Postural Praxis
Test, OPr = Oral Praxis Test,
SPr = Sequencing Praxis Test,
PVC = Praxis on Verbal Com-
mand Test, SV = Space Visualiza-
tion Test, FG = Figure Ground
Test, MAC = Motor Accuracy
Test, DC = Design Copying Test,
CPr = Constructional Praxis
Test. ADOS = Autism Diagnos-
tic Observation Schedule 2nd
Edition, SA = Social Affect,
RRB = Restrictive and Repetitive
Behaviors, D-1 = Sensory Item on
ADOS2.

ADOS-2 Severity scores ranges from 5 to 10 with a mean calculated Cronbach’s alpha to explore the relationship of
score of 8.1 (1.58); and D-1 Score ranged from 0 to 3. Box the grouped tests to the proposed construct. Of note, we did
Plots showing the range of ADOS-2 scores are displayed in not expect to find high correlations among tests, as each test
Fig. 1. is designed to measure a unique function(s). We found that
the tactile tests had significant correlations with each other
SIPT Scores (FI and MFP r = .34, p > .01, FI and GRA r = .41, p > .01; FI
and GRA r = .32, p > .05); as did the praxis tests (PPr and
As shown in Table  3; Fig.  1, SIPT group mean z scores OPr r = .54, p > .01; PPr and SPr r = .46, p > .01; PPr and
ranged from − 3.0 to + 2.0, with SWB, PVC, PPr, and OPr PVC r = .48, p > .01; OPr and SPr r = .53 p > .01; and OPr
showing the lowest mean z scores (-2.64, -2.35, 02.37, and and PVC r = .32, p > .05; SPr and PVC r = .45, p > .01). The
− 2.20 respectively). For reference, in normed samples, by Cronbach’s alpha for tactile and praxis composites were
definition, the average z score is 0, with ± or – 1.0 SD falling α = 0.62 and α = 0.70 respectively. The visual tests showed
within the typical range and below − 1.0, indicating below- moderate correlations among tests (ranging from r = .19
average performance. The group mean scores fell below − .49) and α = 0.66 for Visual Composite. The tests grouped
− 1.0 on all the individual tests except for FI (-0.97), which in the vestibular-proprioceptive and bilateral composite
approached − 1.0. The number of participants for each test were not highly correlated with each other (with the excep-
varies as some participants were not able to complete spe- tion of BMC and KIN- r = .40). The Cronbach’s alpha for
cific tests, with the KIN test having the lowest n (n = 63 Vestibular-Proprioceptive and Bilateral Composite α = 0.43.
out of 93 participants) and the FG test having the highest
n (n = 93 out of 93 participants). Thus, mean scores of the Tactile Perception
group represent those who completed the test. These and
percentage of those with scores below − 1.0 (last column in The mean z scores on the three tactile perception tests com-
Table 3) are presented. prising the tactile perception composite score for the group
To provide information about internal consistency are below − 1.0, with the exception of FI, that approaches
among the SIPT tests grouped into composite scores, we − 1.0 (M = − 0.97, SD = 1.32), as shown in Table 3. In terms
examined correlations among tests in a given composite and of percentage of the sample that scored below − 1.0 (shown

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Journal of Autism and Developmental Disorders

Table 4  Spearman Correlations Among SIPT Composite Scores and Table 5a  Correlations of SIPT and Full Scale IQ Scores
ADOS Scores SIPT Test R value
Tactile Praxis Vestib-Prop Visual MFP .46**
ADOS SA (Calibrated) .043 − .07 .08 − .15 FI .40**
ADOS RRB (calibrated) .06 .07 − .03 − .01 GRA .51**
ADOS Severity Score .05 − .08 .03 − .14 Tactile composite .57**
ADOS D-1 − .14 − .22* − .24* − .15 KIN .16
* Correlation is significant at the 0.05 level Vestib-Prop = vestibular, SWB 34*
proprioceptive and bilateral integration composite BMC .52**
Vestibular composite .53**
in last column of Table 3), of the 89 participants that com- PPr .49**
pleted the MFP, 69% participants scored less than − 1.0 z OPr .40**
score, 78% scored below − 1.0 z score on the GRA test, and SPr .53**
46% scored below − 1.0 on FI. PVC .57**
For the tactile composite score (FI + GRA + MFP), 67% Praxis composite .62**
SV .32*
of the sample scored in the deficient range. The mean z
FG .50**
score was also in the deficient range (M = -1.58, SD = 1.02).
MAC .40**
As shown in Table  4, the tactile composite score was not
DC .42**
significantly related to the ADOS-2 scores. CPr .55**
c .60**
Praxis ** p ≤ .001; * p ≤ .05

There are four praxis tests and a praxis composite score. As


shown in Tables 3 and 69–92% participants scored substan- Visual Perceptual and Visual Motor Skills
tially below − 1.0 on the praxis tests. On PPr, 92% scores
below − 1.0, 88% on OPr, 69% on SPr, and 86% on PrVC, These include five tests of visual perception and visual
with all of participants falling below − 1.0 z score on each motor skills. In general, about half of the sample scored
test. As shown in Table 3, the mean z score for PPr = -2.37 below − 1.0 on these tests. For DC, 61% participants scored
(0.89), OPr mean z score = -2.2 (0.93), SPr mean z score = below − 1.0, SV 59% scored below − 1.0, FG 57% scored
-1.57 (1.25) and PrVC mean z score = -2.35 (1.06). below − 1.0, and MAC where 47% scored below − 1.0, and
For the praxis composite score (PPr + OPr + SPr + PVC) CPr 52% scored below − 1.0. Group mean scores on DC (M
92% of the sample fell below − 1.0 SD, with a mean z score = -1.37, SD = 1.50), SV (M = -1.25, SD = 1.03), DC (M =
of-2.14 (SD = 0.76). The Praxis composite score was not -1.05, SD = 1.07), MAC (M = -0.84, SD = 1.36), and CPr (M
significantly related to the ADOS-2 SA, RRB, or Severity = -1.07, SD = 1.3). 54% of the sample scored below − 1.0 on
scores, but the correlations between the praxis composite the Visual Composite Score (SV + FG +, MAC + DC + CPr)
score and ADOS D-1 approached significance (r= -0,22, with a mean z score = -1.07 (SD = 0.84). The Visual Percep-
p = .06). tion and Visual Motor Composite score was not related to
the ADOS-2 scores.
Vestibular, Proprioceptive and Bilateral Motor Skills
IQ and SIPT Tests
These include three tests: Kin, SWB, and BMC, and a com-
posite score. Of note, 97% of the sample scored below − 1.0 In regard to the relationship of SIPT tests to IQ scores,
on the SWB test. 59% of the sample scored below − 1.0 on as shown in Table  5a, there were significant relationships
KIN, and 57% scored below − 1.0 on BMC. Mean scores for among all but two of the SIPT tests (KIN and PRN). To
the group are as follows: Kin (M =-1.42, SD = 1.21), BMC further explore this relationship, a secondary analysis was
(M = -1.04; SD = 1.02), SWB (M = -2.64, SD = 0.64). conducted. In this analysis, SIPT scores below − 1.0 in three
On the Vestibular, Proprioceptive and Bilateral Motor groups of participants were included: those with full-scale
Skills Composite score (Kin + SWB + BMC), 87% of IQ lower than 85 (n = 44), in the range of 85–115 (n = 43),
the sample fell below − 1.0 with group mean z score = and those above 115 (n = 6). These data are presented in
-1.78 (SD = 0.7). This composite score was not related to Table 5b. While those in the lower IQ group tend to show a
the ADOS-2 SA or RRB but the ADOS-2 D1 scores was higher percentage of lower SIPT scores in many of the tests,
negatively correlated with the vestibular composite score this is not the case across the board. Those with IQ scores
(r = − .24; p = .03). between 85 and 115 and above 115 also show substantial

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Journal of Autism and Developmental Disorders

Table 5b  SIPT by IQ Scores


IQ lower than 85 IQs IQ between 85–115 Upper IQs
N below − 1, % of sample N below − 1, % of sample N below − 1, % of
out of total (all below − 1 out of total (all below − 1 out of total sample
below and above below and above (all below and below
− 1) − 1) above − 1) − 1
SIPT Manual Form Perception (MFP) 35/41 79.55% 23/42 53.49% 3/6 50.00%
SIPT Finger Identification (FI) 24/36 54.55% 12/41 27.91% 2/4 33.33%
SIPT Graphesthesia (GRA) 29/31 65.91% 29/41 67.44% 2/5 33.33%
SIPT Kinesthesia (KIN) 18/24 40.91% 21/40 48.84% 2/5 33.33%
SIPT Standing Walking Balance (SWB) 43/43 97.73% 41/43 95.35% 5/6 83.33%
SIPT Bilateral Motor Coordination 34/42 77.27% 16/43 37.21% 2/6 33.33%
(BMC)
SIPT Postural Praxis (PPr) 41/42 93.18% 38/43 88.37% 5/6 83.33%
SIPT Oral Praxis (OPr) 38/41 86.36% 36/41 83.72% 5 83.33%
SIPT Sequencing Praxis (SPr) 37/41 84.09% 23/43 53.49% 2/6 33.33%
SIPT Praxis on Verbal Command 40/41 90.91% 35/43 81.40% 2/6 33.33%
(PrVC)
SIPT Space Visualization (SV) 31/43 70.45% 21/43 48.84% 2/6 33.33%
SIPT Figure-Ground (FG) 33/44 75.00% 17/43 39.53% 3/6 50.00%
SIPT Motor Accuracy (MAc) 27/42 61.36% 16/43 37.21% 0/6 0%
SIPT Design Copying (DC) 29/41 65.91% 21/43 48.84% 5/6 83.33%
SIPT Constructional Praxis (CPr) 30/41 68.18% 16/43 37.21% 1/6 16.67%
IQ = Full Scale scores
PRN tests are not reported because scores below − 1.0 and above + 1.0 are indicative of dysfunction

percentages of deficits in many of the SIPT tests. For exam- data beyond parent/proxy reported observation of behav-
ple, 5 of the 6 participants (in the IQ above 115 group scored ioral responses to sensation.
in the deficient range (below − 1.0) on SWB, PPr, and OPr. Autism has been defined as a disorder of social commu-
Similarly, a substantial percentage in the IQ group between nication and restricted and repetitive behaviors (APA 2013),
85 and 115 scored below − 1.0 on these tests. Thus, although however, the scientific and clinical autism community rec-
IQ is related to SIPT scores, it does not appear to be the sole ognizes that ASD has additional important features that
influence. impact behavior and function and are critical for develop-
ing effective treatments. The findings from this study sug-
gest that it may be valuable to expand the sensory features
Discussion considered under the restricted and repetitive behaviors
designation, showing that sensory integration challenges
In this paper, the sensory integrative functions in a sample beyond sensory reactivity are often present. Significantly,
of children with ASD are reported. Our approach uses direct the domains identified through the SIPT as particularly vul-
measurements from a normed and validated instrument, the nerable in this sample have shown that they are amenable
SIPT. These data show that autistic children in this sample therapeutic interventions (Schaaf, et al., 2014; Steinbrenner,
have sensory-related differences beyond those described in et al., 2020). Thus, it is important to recognize these features
the DSM-5. Most strikingly, they show deficits in tactile of ASD when they are present. The SIPT represents one way
perception, proprioception, balance, and praxis. These find- to do this.
ings add important knowledge regarding the sensory differ-
ences in ASD and point to the need for a more thorough Praxis
assessment of sensory integrative factors to understand the
full range of sensory factors and their contribution to the In the area of praxis, a substantial number of the partici-
core behavioral phenotype of ASD and provide additional pants scored well below age expectancy on all tests. Praxis
details regarding the specific sensory functions to consider involves the ability to use sensory information to success-
when designing individualized interventions. Importantly, fully act and interact (Ayres, 1989; Edwards et al., 2019;
the SIPT extends well beyond hypo- or hyper-reactivity and Machado et al., 2010; Wolpert et al., 1998). Praxis is more
provides a method of assessing additional sensory factors. It than motor skills; it is a sensorimotor function that depends
also provides performance-based assessment that provides on adequate perception of sensations to direct and guide

13
Journal of Autism and Developmental Disorders

motor actions (Ayres, 1989; Berger, 2012). Children in this balance (Travers et al., 2020; Travers et al., 2013; Lim et
sample had substantial difficulties with all areas of praxis al., 2017). Further research shows that postural and balance
including body imitation praxis (PPr body and OPr face/ difficulties are related to other autism features such as social
mouth), imitating a sequence of novel hand actions (SPr) and communication (Travers et al., 2013) and repetitive behav-
executing novel postures and actions in response to simple iors (Radonovich et al., 2013). Again, these data point to the
verbal directions (PrVC; e.g.: “put one hand on your head importance of assessment of sensory integrative functions
and one hand on your stomach”). These findings are consis- to obtain a comprehensive understanding of autism and to
tent with MacNeil and Mostofsky (2012), who showed that guide tailored interventions designed to improve function
children with ASD, in comparison to those with ADHD and and participation in daily activities and tasks.
typically developing, performed significantly worse on tests
of praxis. These findings suggest that sensory-related praxis Tactile Perception
difficulties may be specific to autism.
Praxis is the foundation for important skills and func- Difficulties in tactile perception, an area that is rarely
tional abilities, including social interactions. As early as assessed in ASD, were found. Usually, sensory testing
2003, Rogers and colleagues (2003) showed that children includes evaluation of tactile reactivity (e.g., hypo and
with ASD had significantly greater difficulties in motor hyper-reactivity) but does not include testing about identi-
imitation in comparison to those with other neurodevelop- fication and localization of tactile sensations. Touch is one
mental disorders and typically developing controls and sug- of the earliest senses to develop, playing a critical role in
gested that motor imitation may provide a foundation for human development across the lifespan (Ayres, 1964; 1972;
social connectedness. Later, Smith-Roley and colleagues Field, 2010; Linden, 2016; Montagu, 1986). The interpreta-
(2015) showed substantial difficulties in praxis, measured tion of touch sensations is critical to human functioning and
using the SIPT, in a cohort of children with ASD, and found is essential for using one’s body effectively in the physical
that low scores on praxis tests were significantly associated world, communicating nonverbally, and sustaining social
with difficulties in social participation. Similarly, Dziuk, relationships (Ayres, 1972; Cascio, et al., 2019; Montagu,
et al. (2007) showed that praxis in children with ASD was 1986). Tactile perception provides essential sensory infor-
correlated with social impairments and suggested that dys- mation that informs social communication (Ellingsen et al.,
praxia “may be a core feature of autism or a marker of the 2016), body awareness (Head, 1920; Tresilian, 2012), pos-
neurological abnormalities that underlie the disorder” (p tural control (Hadders-Algra & Carlberg, 2008), and motor
734). Thus, our data adds to a growing body of literature performance (Shumway-Cook & Woolacott, 2007). In their
showing (1) that children with ASD have deficits in praxis, review, Zetler et al. (2019) found a high prevalence of tac-
(2) these are associated with underlying sensorimotor fac- tile perceptual problems in young children with ASD and
tors, and (3) difficulties in praxis may be an important factor concluded that assessment of tactile perception is an impor-
impacting social participation in children with ASD. In fact, tant part of a comprehensive evaluation.
some scientists now suggest a cognitive-motor model of It is widely recognized that tactile perception informs
autism that appreciates this sensory integrative component awareness of the body by specifying information to the
of ASD (Berger, et al., 2012; Rizzolatti and Fabbri-Destro, somatosensory cortex (Robbe, 2018). Knowing where the
2010; Mostofsky and Ewen, 2011). body was touched or what the body is touching allows dis-
crimination of objects, shapes, and textures (Wolfe et al.,
Postural Control and Balance 2017). Furthermore, touch integrates with other senses, such
as vision, vestibular, and proprioception, to guide actions
Another important finding in these data is that almost all of (Ernst & Banks, 2002) and enable participation in activities
the children in the sample showed difficulties in postural that require seeing, reaching, touching, and moving (Streri
control and balance as measured by the SIPT Standing and et al., 1993). The speed and accuracy of tactile processing,
Walking Balance Test. This test challenges the child’s static as well as the integration of tactile input with other sensory
and dynamic balance requiring them to stand on one foot data, affects the ease and efficiency of actions such as writ-
with eyes open and closed, walk heel to toe, balance on a ing and drawing, manipulating buttons, or finding keys in
half-dowel, and walk on a line. The postural adjustments a bag. Thus, tactile perception is critical for the develop-
needed to maintain balance require integration of vestibular, ment of many foundational skills that impact participation
visual, proprioceptive, and tactile information for the execu- in tasks and interactions with others, contributing to the
tion of adaptive postural and equilibrium responses (Bojanek development of body scheme, motor planning ability, and
et al., 2020). Our findings are consistent with the literature motor skill acquisition. Specifically, in regard to ASD and
showing that autistic persons have greater challenges in tactile perception, Cascio and colleagues (2015) showed

13
Journal of Autism and Developmental Disorders

that parent-reported tactile hyporeactivity in children was evident, even when IQ was considered, albeit these were
associated with a later event-related potential in the somato- not as severe as the other areas. As shown in Table 5, those
sensory cortex suggesting delayed processing; and Puts et with IQ scores above 115 show deficits in visual perception
al. (2014) found that children with ASD had higher detec- and visual motor skills, as do the other IQ groups. It has
tion threshold (decreased reactions) to tactile stimulation been suggested that autistic persons may have strength in
providing evidence that decreased tactile perception in attending to the details of the visual environment but chal-
ASD may be related to differences in neural processing of lenges in global processing or “seeing the forest from the
touch sensations. Others, however, suggest that decreased trees” (Robertson and Baron-Cohen, 2017) and “difficulty
tactile perception may reflect more conservative decision- integrating dynamic (less predictable) visual information
making in children with ASD (Quinde-Zlibut et al., 2020). into motor commands” (Lim and Mostofsky, 2022; page
Clearly, more research is needed to clarify the neural basis 99). Further, visual motion perception may evolve more
of decreased tactile perception in ASD. slowly in ASD (Robertson, et al., 2012; Robertson, et al.,
Further, tactile perception is related to praxis. In multiple 2014). These authors suggest that visual motion percep-
studies across six decades, Ayres and colleagues showed tion may impact the acquisition of crucial motor, social and
strong and significant associations between tactile percep- communicative development. While it is beyond the scope
tion and praxis (Ayres, 1964, 1965, 1972, 1989; Mulligan, of this paper to examine the relations of visual perception
1998; Mailloux, et al., 2011). This relationship may explain and visual motor skills to later development in ASD, our
why children who have poor tactile perception often have findings point to the need for further analysis of these skills
trouble planning actions in daily life activities, such as don- and their role in autism.
ning clothing, playing with toys, or using a writing utensil.
Poor tactile functions in children can also impair the devel- A case for Measuring Sensory Integration
opment of fine motor skills, in-hand manipulation, and tool
use. These functions are needed for success in play, self- It is interesting to note that the SIPT composite scores were
care, and academic tasks (Ayres, 2005; Case-Smith, 1991). not strongly correlated with the ADOS-2 SA scores or the
Ayres (2005) noted this relationship between touch and ADO-2 S RRB scores. This finding suggests that the SIPT is
praxis, stating that, “… tactile input-particularly sensations measuring a unique aspect of ASD that is not captured with
from the hands, fingers, and mouth are very specific…A the ADOS-2. The SIPT provides a useful, standardized, and
detailed picture is formed of these sensations in the sensory norm-referenced assessment of these important but often
cortex, and the person can respond in a very precise way. neglected sensory integrative functions. One hesitation to
Writing is a good example of an activity that involves many using the SIPT with ASD children is concern that they may
specific tactile sensations…” p. 92. Hence, tactile percep- not be able to complete the test battery. By design, the SIPT
tion provides a foundation for praxis. In our sample, many utilizes simple verbal and physical instructions (i.e., “use
participants showed both tactile perception, praxis difficul- your pencil to copy these designs” or “make your body do
ties, and delays in daily living skills. Given that tactile per- what I am doing”), making it appropriate for children with
ception provides important foundations for engagement in ASD who have low language abilities or cognitive skills.
many tasks and activities, it is crucial that it be assessed All ninety-three participants randomized in this study par-
when considering the sensory factors that may impact par- ticipated in at least 70% of the SIPT tests, and 66% com-
ticipation in tasks and activities. pleted all 17 SIPT tests. Given that participants IQ scores
ranged from 50 to 166, our findings show that the SIPT
Visual Perception and Visual Motor Skills can be used with a wide range of ASD children, including
those with low IQ scores. Eight participants had full-scale
While neuropsychological tests measure visual perceptual IQ scores below 70 and of these, two had non-verbal IQ
function and visuoconstructive abilities with tasks utiliz- that fell below 60. All eight of these participants were able
ing spatial relationships, visual scanning, and visual dis- to complete the SIPT. Further, it appears that although IQ is
crimination, the SIPT is unique in measuring these specific related to SIPT scores, it is not the sole determinant of these
functions as well as integrated sensory perception and sen- scores, as even children with IQ scores above 85 showed
sorimotor skills such as praxis and balance (Korkman et al., difficulties.
2007; Lezak et al., 2012; Roid & Miller, 1997). In terms of Of note, to make testing of these sensory integrative
visual perception and visual motor skills, Smith-Roley, et functions even more accessible, a new test is in the final
al. (2015) showed that autistic children exhibited relative stages of development. The Evaluation of Ayres Sensory
strength in visual-related skills. In our sample, however, dif- Integration (EASI; (Mailloux, et al. 2020)) evaluates similar
ficulties with visual perception and visual motor skills were functions as the SIPT, but includes updated norms, extends

13
Journal of Autism and Developmental Disorders

the normative age groups to a wider range (3–12 years of This approach is supported by the fact that normative data
age), and is available in an open-source format. This test on the SIPT plateau at the 8.11 age range. However, it is
will provide an updated option for testing sensory integra- possible that the SIPT z scores for the 9-year-olds may be an
tive functions. Training on the EASI is available online and underestimation of their actual performance (i.e. scores may
in more than 10 languages making it accessible to a wide be worse than reported). Finally, it should be noted that the
range of countries and cultures. norms for the SIPT are somewhat dated in that they are from
In summary, this study adds to the growing body of lit- 1989 and, thus, may not be representative of the population
erature showing that children with ASD who are identified today. This is one reason that the EASI is being developed,
with sensory issues show additional sensory integrative and future analysis of sensory functions in ASD can use this
difficulties beyond those named in the DSM5 and beyond assessment.
those measured by questionnaires designed to assess the
presence of sensory differences such as the Sensory Profile Acknowledgements  We thank the children and families who partici-
pated in this study, and Drs. Joanne Hunt, John Eboli, and Anna Keen-
(Dunn, 2014), the Sensory Processing Measure (Parham, aghan, who served as independent evaluators. This study was funded
et al., 2007) and the Sensory Experiences Questionnaire by the National Institute of Child Health and Human Development
(Baranek, 2005). Our findings highlight the value of testing Clinical trial number (NICHD #RO1HD082814). Dr. Zoe Mailloux is
these important functions to obtain a comprehensive view an of the authors of the Evaluation of Ayres Sensory Integration.
of the child’s sensory integrative strengths and challenges
for characterization and personalization of treatment. Often Declarations
sensory testing is limited to parent report of sensory reactiv-
Conflict of interest  Dr. Mailloux is an author of the Evaluation of
ity (hypo, hyper-reactivity, seeking). While this is a valu- Ayres Sensory Integration which is mentioned in this article.
able aspect of sensory assessment, this approach may miss
important sensory integrative aspects (e.g., tactile percep-
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