Skip to main content
NCBI home page
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2023 May 1.
Published in final edited form as: Disabil Rehabil. 2022 Mar 10;45(5):848–856. doi: 10.1080/09638288.2022.2043946

Pain sensitivity and perceptual sensitivity are associated with severity of emotional dysregulation in children with ADHD: a cross-sectional analysis using the Temperament in Middle Childhood Questionnaire

Alisha M Bruton a, Angela Senders b, Gabriella Tost a, Hayleigh Ast a, Lisa M Robinette c, Brenda Leung d, Irene E Hatsu c, L Eugene Arnold e, Jeanette M Johnstone a,f
PMCID: PMC9463405  NIHMSID: NIHMS1789129  PMID: 35271401

Abstract

Purpose:

Nearly 50% of children with attention-deficit/hyperactivity disorder (ADHD) experience emotional dysregulation or sensory over-responsiveness; this study examines their association.

Methods:

This cross-sectional analysis (n = 124) used data from the Micronutrients for ADHD in Youth (MADDY) Study, which enrolled children aged 6–12 with ADHD and emotional dysregulation. Sensory responsiveness was assessed using two subscales from the factor-analyzed Temperament in Middle Childhood Questionnaire: Pain Sensitivity and Perceptual Sensitivity. Emotional dysregulation was assessed using the Emotional-Problems and Conduct-Problems subscales from the Strengths and Difficulties Questionnaire and a composite score from the Child & Adolescent Symptom Inventory-5. Multivariable linear regression measured the association of pain and perceptual sensitivity with the severity of emotional dysregulation.

Results:

In adjusted models, pain sensitivity was positively associated with Emotional Problems (β = 0.97; 95% CI: 0.52, 1.41; p < 0.0001), Conduct Problems (β = 0.83; 95% CI: 0.44, 1.21; p = 0.0001), and CASI-5 composite (β = 0.25; 95% CI: 0.16, 0.34; p < 0.0001). Perceptual sensitivity was positively associated with Emotional Problems (β = 0.75; 95% CI: 0.15, 1.35; p = 0.01) but not Conduct Problems (β = 0.27; 95% CI: −0.24, 0.77; p = 0.30) or CASI-5 composite (β = 0.12; 95% CI: −0.01, 0.24; p = 0.07).

Conclusion:

Pain sensitivity was associated with the severity of emotional dysregulation in this ADHD sample. To better understand possible causal links, longitudinal studies are warranted.

Keywords: ADHD, attention, emotion regulation, irritability, anger, pain, sensory sensitivity, over-responsiveness

Introduction

Attention-deficit/hyperactivity disorder (ADHD) affects approximately 8% of children in the United States [1]. Current criteria from the Diagnostic and Statistical Manual of Mental Disorders, version 5 (DSM-5) identifies three hallmark ADHD symptoms: inattention, hyperactivity, and impulsivity [2]. However, up to half of the children with ADHD exhibit emotional dysregulation, including anger, tantrums, irritability, or aggression [3,4]. Children with ADHD and emotional dysregulation experience more challenges in family life, social relationships, and academic performance than those with ADHD alone [5]. Although emotional dysregulation increases impairment in ADHD, the drivers of emotional dysregulation remain poorly understood [4,6].

One potential contributor to emotional dysregulation is sensory over-responsiveness, defined as an exaggerated or prolonged response to pain or other sensation [7]. Sensory over-responsiveness occurs in 5% of typically-developing children [8] but up to 50% of children with ADHD [9,10]. One theoretical model posits that exaggerated reactions to sensations and pain may have a detrimental impact on an individual’s emotional state [11]. Research in children with irritable or aggressive behavior supports this theory, suggesting that heightened sensitivity to sensation or pain may provoke irritability or aggression [12–14].

To date, no studies in children with ADHD have assessed pain sensitivity and emotional dysregulation. Several studies have assessed sensitivity to sensation (including sight, sound, touch, smell and taste; called perceptual sensitivity) and emotional dysregulation in ADHD, though results are conflicting [15–17]. Two studies in children with ADHD found an association between emotional dysregulation and some measures of perceptual sensitivity, but not others [15,17]. A third study found perceptual sensitivity moderated the relationship between ADHD symptoms and emotional dysregulation, but did not report the association between perceptual sensitivity and emotional dysregulation itself [16].

Perceptual sensitivity can negatively impact psychosocial development [18,19], participation in daily life activities [20], and academic performance [21,22]. Heightened pain sensitivity can negatively impact mental health [23,24] and increase the risk of physical injury [25]. Understanding how sensory over-responsiveness impacts emotional dysregulation in ADHD may facilitate early identification of impairment risk and highlight an opportunity for targeted treatment. Therefore, we investigated the relationship between the severity of emotional dysregulation and sensory over-responsiveness in children with ADHD. We hypothesized that sensory over-responsiveness would be positively associated with the severity of emotional dysregulation.

Methods

Data source and study sample

This cross-sectional study was conducted with data collected at the baseline visit of the Micronutrients for ADHD in Youth (MADDY) study. The MADDY study was a 3-site (Oregon Health & Science University, Ohio State University, and the University of Lethbridge in Alberta, Canada) randomized placebo-controlled trial designed to assess the effect of a broad-spectrum micronutrient supplement on symptoms of ADHD and emotional dysregulation in a pediatric population. Families with children 6–12 years old were recruited through schools, hospitals, and referrals from mental health providers and pediatricians between 2018 and 2020. Participants met DSM-5 criteria for ADHD as assessed by the Child and Adolescent Symptom Inventory, version 5 (CASI-5) parent-report questionnaire. In addition, at least one symptom of emotional dysregulation on the Oppositional Defiant Disorder (ODD) or Disruptive Mood Dysregulation Disorder (DMDD) subscales of the CASI-5 were required. For example, a parent must have endorsed their child was angry or irritable most of the day, frequently lost their temper, often argued with adults, or frequently took their anger out on others. Of the 384 participants screened, 135 were enrolled.

At baseline, parents or guardians (hereafter parents) completed a comprehensive set of parent-report questionnaires about their child’s health and symptoms. The detailed methods for the MADDY study are provided elsewhere [26,27]. All parents/guardians provided consent and children provided assent using forms and procedures approved by Institutional Review Boards at each participating institution. The study was registered with the National Clinical Trials Registry (NCT03252522).

Dependent variables: emotional dysregulation

The severity of emotional dysregulation was assessed using three parent-report measures: two from the Strengths & Difficulties Questionnaire (SDQ) and one from the CASI-5.

The SDQ is a validated 25-item Likert-type questionnaire used to assess emotional and behavioral problems in children. Two subscales were used: Emotional Problems and Conduct Problems [28] which have been validated for the assessment of ADHD and emotional dysregulation [29,30]. Subscale scores were obtained by summing the Likert responses (on a 0–2 scale) across questions. Total subscale scores range from 0 to 10; a higher score indicates more of the symptom in question. Each of the subscale scores was evaluated as a continuous variable.

The CASI-5 is a validated questionnaire with multiple subscales that reflect the DSM-5 criteria for a particular disorder [31,32]. In this study, we combined subscales of Inattention, Hyperactivity/Impulsivity, ODD, DMDD and Peer Conflict into a composite score. This composite scoring method was previously developed to assess emotional dysregulation in the context of ADHD [33]. The subscales contain 2–9 items that ask parents to endorse how often a child experiences a particular symptom, and how impairing that symptom is to everyday functioning. The Likert-type answers were averaged to create subscale scores, and the subscales were combined into a composite score with a range of 0–3. Higher scores indicate more symptoms. The CASI-5 composite score was evaluated as a continuous variable.

Independent variables: sensory over-responsiveness

Sensory over-responsiveness was assessed with the Temperament in Middle Childhood Questionnaire (TMCQ), a validated, parent-report, 157-item Likert-type questionnaire used to assess childhood temperament [34]. Two of the nine subscales identified in a confirmatory factor analysis [35] were used: Pain Sensitivity and Perceptual Sensitivity, which consisted of seven and ten items, respectively. The total score for each subscale is a mean of the subscale items (range 1–5). A higher score indicates higher levels of either pain or perceptual sensitivity. Each subscale was evaluated as a continuous variable.

The Pain Sensitivity subscale items ask parents to rate the child’s response to pain, for example how likely is the child to cry when only a little bit hurt, or if the child would be very upset by a little cut or bruise. The Perceptual Sensitivity subscale items ask about the degree to which the child notices small changes in their environment, such as the brightness of light, odors, or the sound of birds.

Other independent variables, including age (continuous), sex (parent-reported male or female), and study site (Oregon, Ohio, Canada) were adjusted for in analyses. The race variable was considered for inclusion as a proxy for social stressors that participants may be exposed to [36]; we collapsed race into White or Another Race due to small sample sizes. Season of enrollment (spring, summer, autumn, winter) was considered to account for changes in symptoms due to home or school environment, e.g., being on summer vacation at the time of the baseline visit. Associations exist between season and mood in adults [37].

Statistical analysis

Characteristics of the study participants were examined for possible confounds using descriptive statistics. The distribution of participant characteristics across quartiles of each independent variable was assessed using ANOVA for continuous variables, Pearson’s chi-square test for categorical variables, and Fisher’s exact test for categorical variables with a low number of expected values. Categorizing continuous variables into quartiles allows examination of extreme values and specific differences between groups. To determine how clinically significant the ASD symptoms were in our sample, scores were compared to normative sample data [31]. A score in the 70th percentile or above is considered to indicate clinically relevant symptoms that may warrant a clinical evaluation [31].

Multiple linear regression with ordinary least squares (OLS) was used to estimate six unstandardized β coefficients and 95% confidence intervals (CIs) as the measure of the association between each of two sensory over-responsiveness variables and each of three emotional dysregulation variables. All six models were adjusted for age, sex, and study site. Additional variables including race and season of enrollment were assessed for model inclusion using the 10% change in estimation method [38]. These variables were assessed by adding each of them to the adjusted model one at a time. If this resulted in ≥10% change in the β coefficient, the variable was considered a confounder. After confounders were identified, they were added sequentially to the model to see if they remained a confounder in the presence of the other variables. The process was repeated separately for all six models. This method allowed for the inclusion of season of enrollment as a covariate in all models. Data were evaluated for violations of the assumptions of OLS regression using statistical and graphical methods (Supplemental materials) [39–41]. Violations of the assumption of homoscedasticity were addressed by using robust standard errors [42].

To check for formal interactions between sex and independent variables, a cross-product term of these variables was included in the adjusted model. All hypothesis tests were two-tailed; a value of α < 0.05 was considered statistically significant. The Benjamini-Hochberg procedure was used to correct for multiple comparisons with a false discovery rate of 0.05 [43].

Participants were excluded if they were missing data for the independent or dependent variables (n = 20). Differences in demographic or dependent variables between those who had and did not have missing data were evaluated.

Sensitivity analyses

The CASI-5 composite score is a validated method for assessing emotional dysregulation in children with ADHD, however, the score includes ADHD symptoms. Since this analysis is focused on the association between sensory over-responsiveness and severity of emotional dysregulation, and not directly on ADHD, a modified composite score was created excluding the items on inattention and hyperactivity and using only the ODD, DMDD, Peer Conflict, and Impulsivity subscales. The association of pain and perceptual sensitivity with inattention and hyperactivity were separately assessed before their removal from the original composite score. A planned sensitivity analysis was conducted using this new score, examining its association with pain sensitivity and perceptual sensitivity. Because this modified composite score is not validated, this analysis was considered exploratory.

Hypersensitivity to pain and other sensations is part of the diagnostic criteria for autism spectrum disorder (ASD) [2]. ASD often co-occurs with ADHD [1,44], but was an exclusion criterion for the MADDY study. However, it is possible that children with undiagnosed ASD were included in the sample. Therefore, an unplanned stratified analysis was conducted to examine the impact of ASD symptoms on the results. Participants were divided into quartiles based on the CASI-5 ASD symptom score. Then, the association between pain and perceptual sensitivity and severity of emotional dysregulation was assessed separately for children in the lowest three quartiles (n = 92) and the highest quartile (n = 32) of ASD symptoms.

Power analysis

The sample size was predetermined by the number of complete baseline observations in the MADDY study (n = 124). Therefore, a power analysis was conducted to determine the minimum amount of variance in emotional dysregulation that could be attributed to sensory over-responsiveness. The sample of 124 had 90% power to detect variance (△R2) in emotional dysregulation of at least 6% attributable to sensory over-responsiveness.

The STROBE guidelines were used to guide reporting [45]. An analysis plan was indexed online before the project began; it governed our analyses unless stated otherwise [46]. Statistical analyses were performed with Stata software, version 16.1 [47].

Results

The mean age of participants was 9.8 (1.7) years and 70% were male (Table 1). The participants were approximately equally divided between the three study sites (Oregon, 38%; Ohio, 28%; Canada, 34%). The majority of participants were enrolled in the spring (35%) or summer (33%), with fewer being enrolled in the autumn (21%) or winter (10%). Baseline characteristics of included participants did not differ across quartiles of our primary independent variables, except for sex. Boys were less likely to exhibit symptoms of perceptual sensitivity by parent-report (p < 0.01). Mean symptom severity scores at baseline for the SDQ, CASI-5 and TMCQ are displayed in Table 2. On the 0–3 scale of the CASI-5, mean (SD) ADHD scores were 2.23 (0.49) for inattention and 1.77 (0.66) for hyperactivity-impulsivity. On the 1–5 scale of the TMCQ, mean pain sensitivity scores were 2.74 (0.83), and mean perceptual sensitivity scores were 3.26 (0.69). There was a significant difference by the site in the number of participants with missing data, with the Ohio site missing more than the other two sites (Oregon, 4% missing; Ohio, 26%; Canada, 13%) (Table S3). There were no other differences between participants with and without missing data by demographic or dependent variables.

Table 1.

Demographic characteristics of participants by quartile of each primary independent variable (pain sensitivity, perceptual sensitivity).

Total
N = 124		 Pain sensitivity Perceptual sensitivity
Q1
N = 36		 Q4
N = 29		 p-value Q1
N = 32		 Q4
N = 26		 p-value
Mean age (SD) 9.8 (1.7) 9.9 (1.8) 9.7 (1.8) 0.92 9.6 (1.6) 9.2 (1.8) 0.06
Sex 0.98 <0.01
 Female 37 (30%) 11 (31%) 8 (28%) 12 (38%) 14 (54%)
 Male 87 (70%) 25 (69%) 21 (72%) 20 (62%) 12 (46%)
Study site 0.58 0.62
 Oregon 47 (38%) 15 (42%) 11 (38%) 17 (53%) 9 (35%)
 Ohio 35 (28%) 10 (28%) 5 (17%) 7 (22%) 8 (31%)
 Canada 42 (34%) 11 (31%) 13 (45%) 8 (25%) 9 (35%)
Season of enrollment 0.81 0.91
 Spring 44 (35%) 12 (33%) 9 (31%) 9 (28%) 11 (42%)
 Summer 41 (33%) 12 (33%) 9 (31%) 10 (31%) 9 (35%)
 Autumn 26 (21%) 9 (25%) 6 (21%) 9 (28%) 4 (15%)
 Winter 13 (10%) 3 (8%) 5 (17%) 4 (12%) 2 (8%)
Open in a new tab

Note: SD, standard deviation. P-value is for the difference between all four quartiles and is not corrected for multiple testing.

Table 2.

Mean symptom scores at baseline in children with ADHD and emotional dysregulation (N = 124).

Parent-reported measures (Scale range) Mean (SD)
Strengths & Difficulties Questionnaire (1–10)
 Emotional problems 3.32 (2.38)
 Conduct problems 3.63 (1.89)
Child & Adolescent Symptom Inventory, v5 (0–3)
 Inattention 2.23 (0.49)
 Hyperactivity/Impulsivity 1.77 (0.66)
 Opposition defiant disorder 1.67 (0.70)
 Disruptive mood dysregulation disorder 1.26 (0.86)
 Peer conflict 0.54 (0.55)
 Impairment 1.49 (0.66)
 Autism spectrum disorder (ASD) 0.49 (0.40)
 ASD symptoms ≥ 70th percentile, n (%) 36 (29%)
Temperament in Middle Childhood Questionnaire (1–5)
 Pain sensitivity 2.74 (0.83)
 Perceptual sensitivity 3.26 (0.69)
Open in a new tab

SD, standard deviation.

After adjusting for age, sex, study site, and season of enrollment, pain sensitivity was positively associated with emotional problems (β = 0.97; 95% CI: 0.52, 1.41; p < 0.0001; R2 = 0.21; Table 3). This suggests a one-point increase in pain sensitivity on a 1–5 scale is associated with a one-point increase in emotional problems on a 0–10 scale. Pain sensitivity was also positively associated with conduct problems (β = 0.83; 95% CI: 0.44, 1.21; p = 0.0001; R2 = 0.16) and the CASI-5 composite score (β = 0.25; 95% CI: 0.16, 0.34; p < 0.0001; R2 = 0.26) in adjusted models. All three results retained significance when correcting for multiple comparisons (Table S4).

Table 3.

Pain sensitivity association with three measures of emotional dysregulation among children with ADHD (N = 124).

β 95% CI p-value R 2 ΔR2
Emotional problems
 Crude model 0.98 0.53, 1.43 <0.0001 0.12
 Adjusted model 0.97 0.52, 1.41 <0.0001 0.21
 Adjusted model without pain sensitivity 0.10 0.11
Conduct problems
 Crude model 0.83 0.45, 1.21 <0.0001 0.13
 Adjusted model 0.83 0.44, 1.21 <0.0001 0.16
 Adjusted model without pain sensitivity 0.03 0.13
Composite score
 Crude model 0.24 0.14, 0.33 <0.0001 0.17
 Adjusted model 0.25 0.16, 0.34 <0.0001 0.26
 Adjusted model without pain sensitivity 0.08 0.18
Open in a new tab

Note: CI, confidence interval. The p-value presented is for the β-coefficient and is not corrected for multiple testing. All adjusted models included additional variables of age, sex, study site, and season of enrollment. Emotional Problems and Conduct Problems subscales are from the Strengths and Difficulties Questionnaire (SDQ). The composite score combines six subscales from the Child & Adolescent Symptom Inventory, version 5 (CASI-5).

Perceptual sensitivity was significantly associated with emotional problems in an adjusted model (β = 0.75; 95% CI: 0.15, 1.35; p = 0.01; R2 = 0.15; Table 4). This retained significance when correcting for multiple comparisons (Table S4). Perceptual sensitivity was not significantly associated with conduct problems (β = 0.27; 95% CI: −0.24, 0.77; p = 0.30) nor the CASI-5 composite score (β = 0.12; 95% CI: −0.01, 0.24; p = 0.07). Tests for interaction between sex and pain or perceptual sensitivity were not statistically significant.

Table 4.

Perceptual sensitivity association with emotional dysregulation among children with ADHD (N = 124).

β 95% CI p-value R 2 ΔR2
Emotional problems
 Crude model 0.77 0.17, 1.37 0.01 0.05
 Adjusted model 0.75 0.15, 1.35 0.01 0.15
 Adjusted model without perceptual sensitivity 0.10 0.05
Conduct problems
 Crude model 0.31 −0.18, 0.80 0.21 0.01
 Adjusted model 0.27 −0.24, 0.77 0.30 0.04
 Adjusted model without perceptual sensitivity 0.03 0.01
Composite score
 Crude model 0.11 −0.02, 0.23 0.09 0.02
 Adjusted model 0.12 −0.01, 0.24 0.07 0.10
 Adjusted model without perceptual sensitivity 0.08 0.03
Open in a new tab

Note: CI, confidence interval. The p-value presented is for the β-coefficient and is not corrected for multiple testing. All adjusted models included additional variables of age, sex, study site, and season of enrollment. Emotional Problems and Conduct Problems are subscales from the Strengths and Difficulties Questionnaire (SDQ). The composite score combines six subscales from the Child and Adolescent Symptom Inventory, version 5 (CASI-5).

Sensitivity analyses

The strength of the association between pain sensitivity and the modified CASI-5 composite score (which excluded inattention and hyperactivity symptoms) increased by approximately 20% (β = 0.30; 95% CI, 0.19, 0.41; p < 0.0001; R2 = 0.25; Table 5) compared to the association with the full composite. The strength of the association between perceptual sensitivity and the modified composite score also increased slightly yet remained nonsignificant (β = 0.14; 95% CI, −0.01, 0.29; p = 0.07; R2 = 0.09). Inattention was not associated with pain sensitivity or perceptual sensitivity; hyperactivity was not associated with pain sensitivity but was associated with perceptual sensitivity (β = 0.20; 95% CI, 0.01, 0.39; p = 0.04).

Table 5.

Sensitivity analysis; association between pain sensitivity and perceptual sensitivity and emotional dysregulation using modified CASI-5 composite score.

β 95% CI p-value R 2 ΔR2
Pain sensitivity
 Crude model 0.29 0.18, 0.40 <0.0001 0.18
 Adjusted model 0.30 0.19, 0.41 <0.0001 0.25
 Adjusted model without pain sensitivity 0.07 0.19
Perceptual sensitivity
 Crude model 0.13 −0.01, 0.28 0.07 0.03
 Adjusted model 0.14 −0.01, 0.29 0.07 0.09
 Adjusted model without perceptual sensitivity 0.07 0.03
Open in a new tab

Note: CASI-5, Child and Adolescent Symptoms Inventory, version 5; CI, confidence interval. The p-value presented is for the β-coefficient and is not corrected for multiple testing. All adjusted models included additional variables of age, sex, study site, and season of enrollment. Pain sensitivity and Perceptual sensitivity are subscales from a factor analysis of the Temperament in Middle Childhood Questionnaire (TMCQ).

After assessing the relationship stratified by symptoms of ASD (Table S5) we found that, for children in the lowest three quartiles of ASD symptoms (n = 92), the strength of the associations between pain sensitivity and all three measures of emotional dysregulation were reduced compared to the full dataset (n = 124). Perceptual sensitivity and the three measures of emotional dysregulation were not associated in this subsample. For the children in the highest quartile of ASD symptoms (n = 32), the strength of the association between pain sensitivity and two of three measures of emotional dysregulation was no longer significant. However, the strength of the association between perceptual sensitivity and severity of emotional dysregulation increased in these children compared to the full dataset.

Discussion

The aim of this study was to quantify the association of sensory over-responsiveness, comprised of parent-reported pain sensitivity and other perceptual sensitivity, with the severity of emotional dysregulation in children with ADHD and emotional dysregulation. We observed significant associations of pain sensitivity and perceptual sensitivity with the severity of emotional dysregulation. Pain sensitivity was strongly associated with all three measures of emotional dysregulation, while perceptual sensitivity was significantly associated with one measure, emotional problems.

To our knowledge, this is the first study to assess parent-reported pain sensitivity and severity of emotional dysregulation in children with ADHD. However, one study assessed objectively measured pain sensitivity in boys ages 10–17 with ADHD or ADHD plus conduct disorder (n = 183) [48], which involves callous, unemotional, or defiant behavior [2]. In that study, pain sensitivity was assessed via heat applied to the palm. In that sample, boys with ADHD and conduct disorder had decreased pain sensitivity compared to those with only ADHD, but emotional dysregulation was not assessed. These results suggest that decreased pain sensitivity in ADHD may be associated with callous, unemotional behavior. In contrast, in our sample, we found that increased pain sensitivity was associated with increased severity of emotional dysregulation in children with ADHD. The two studies are too heterogeneous to directly compare results. Speculatively, perhaps high or low pain sensitivity impacts emotional regulation in opposite directions. The differential impacts of pain sensitivity on emotional and behavioral symptoms in ADHD require further study.

We found a significant association between perceptual sensitivity and only one of three measures of emotional dysregulation. Three prior studies also report mixed findings [15–17]. In a cross-sectional study of children with ADHD and healthy controls (n = 56), investigators examined parent-reported sensory symptoms using the Short Sensory Profile (SSP) [17,49]. The SSP includes three subscales that assess perceptual sensitivity: Tactile Sensitivity, Visual/Auditory Sensitivity, and Taste/Smell Sensitivity. The Child Behavior Checklist (CBCL) Aggressive Behavior subscale assessed emotional dysregulation [50]. In the children with ADHD, the Aggressive Behavior subscale was associated with the Tactile Sensitivity subscale (r = 0.66, p < 0.001), but not the Visual/Auditory Sensitivity or Taste/Smell Sensitivity subscales. In another cross-sectional study of children with ADHD and healthy controls (n = 74), investigators assessed children’s symptoms with the parent-reported Sensory Profile (SP) [51] and an earlier version of the CBCL [15,52]. The Oppositional Defiant Disorder (ODD) subscale of the CBCL was used to assess emotional dysregulation. ODD includes anger and irritability [2] and ODD symptoms are often used as a measure of emotional dysregulation. In the children with ADHD, ODD symptoms were associated with the Auditory Processing subscale of the SP (r = 0.40, p = 0.014), but not the Visual Processing, Sensory Sensitivity, or Perceptual Sensitivity subscales. A third cross-sectional study in children with symptoms of ADHD (n = 71) assessed parent-reported symptoms of ADHD, emotional dysregulation, and perceptual sensitivity via the Emotion Regulation Checklist (ERC) and the Sensory Sensitivity subscale of the SSP [16,49,53]. In that sample, perceptual sensitivity moderated the relationship between hyperactivity/impulsivity and emotional dysregulation. The association between perceptual sensitivity and emotional dysregulation was not reported.

These studies highlight the variety of parent-report questionnaires in use on sensory over-responsiveness. Some questionnaires assess sensitivity to the sensation as well as the impact on a child’s emotional state; others attempt to separate these two constructs [54–56]. The TMCQ Pain Sensitivity subscale used in our study measures both physical sensitivity and emotional reactions to pain (Table 6).

Table 6.

Items comprising the pain sensitivity and perceptual sensitivity subscales of the Temperament in Middle Childhood Questionnaire.

Pain sensitivity
 5 Is bothered by pain when s/he falls down.
 30 Cries when given an injection.
 39 Can take a Band-Aid® off when needed, even when painful.*
 63 Is scared of injections by the doctor.
 64 When s/he cries, tends to cry for more than a couple of minutes at a time.
 138 Is quite upset by a little cut or bruise.
 154 Is likely to cry when even a little bit hurt.
Perceptual sensitivity
 36 Notices the color of people’s eyes.
 44 Notices the sound of birds.
 57 Notices odors like perfume, smoke, and cooking smells.
 77 Touches fabric or other soft material.
 95 Likes to look at trees.
 109 Notices small changes in the environment, like lights getting brighter in a room.
 111 Notices things others don’t notice.
 114 Notices even little specks of dirt on objects.
 123 Likes to run his/her hand over things to feel if they are rough or smooth.
 150 Notices when parents are wearing new clothing.
Open in a new tab
*

Item is reverse-scored.

For example, it asks if a child is “quite upset by a little cut or bruise.” This may confound the association between pain sensitivity and emotional dysregulation in our sample, as emotional reactions to pain may present similarly to emotional dysregulation itself. In comparison, the TMCQ Perceptual Sensitivity subscale measures awareness of sights, sounds, and odors but focuses on the awareness that is not distressing or impairing. Examples include asking if a child “Likes to look at trees” or “Likes to run his/her hand over things to feel if they are rough or smooth.” Heightened awareness may not necessarily be impairing if it does not elicit a negative emotional response in the child. This may explain why perceptual sensitivity in this study was associated with only one measure of emotional dysregulation, Emotional Problems.

In addition to the variety of assessment tools in use, there are a number of terms used to describe the construct of sensory over-responsiveness. These include tactile defensiveness [57], tactile sensory dysfunction [58], sensory responsivity [59], sensory modulation dysfunction/disorder [17,60], sensory processing problems [61], sensory processing sensitivity [62], and atypical sensory profiles [63]. There is no agreed-upon definition of sensory over-responsiveness or gold standard by which to assess it. This lack of standardization makes the comparison between studies difficult. Developing standardized definitions and measurement tools is crucial in order to understand the relationship between sensory over-responsiveness and emotional dysregulation. For example, the level of sensory over-responsiveness may predict response to treatment [64].

Objective measures may complement parent-report questionnaires to provide a more robust picture of sensory symptoms among children, especially when it comes to pain. Emerging evidence suggests that sensory over-responsiveness is associated with physiological differences which can be measured with brain imaging and other objective measures. Small studies suggest that sensory over-responsiveness may be partially explained by differences in skin conductance or vagal tone [9,65,66] and over-responsiveness is associated with greater sensitivity to experimental pain [67–69]. Brain imaging demonstrates that boys with sensory over-responsiveness have structural differences in white matter, suggesting a biological basis for the disorder [70].

Sensory over-responsiveness is a modifiable treatment target, but longitudinal studies are needed to assess its effect on emotional dysregulation in ADHD. An occupational therapy technique called sensory integration has been widely studied in children with sensory over-responsiveness [71]. Studies have reported improvements in sensory symptoms, disruptive behavior, and attention in children following sensory integration interventions [72–77]. In one study, post-intervention, children exhibited less impairment in self-care activities and social functioning, requiring less caregiver support [78]. However, studies did not assess emotional dysregulation, although sensory integration has been shown to improve emotion regulation in healthy adults [79]. No studies have been done specifically in children with ADHD. Longitudinal studies are needed to assess the temporal association between sensory over-responsiveness and emotional dysregulation. If sensory over-responsiveness contributes to emotional dysregulation in ADHD, sensory integration interventions could modify sensory over-responsiveness and potentially improve emotional dysregulation.

To better characterize the factors that comprise sensory over-responsiveness, we conducted a sensitivity analysis. The results suggest that pain and perceptual sensitivity are associated with the severity of emotional dysregulation in children with ADHD and that symptoms of inattention do not contribute to this association. Hyperactivity symptoms, however, might contribute to perceptual sensitivity. Our results contradict another study which found perceptual sensitivity was correlated with inattention (r = −0.42; p = 0.01), but not hyperactivity (r = −0.09; p = 0.62) in children with ADHD [15]; yet they align with another that found a positive association with hyperactivity only (β = 1.39; p < 0.001) [16]. Differences in the way perceptual sensitivity is assessed may account for these conflicting results.

Sensory hypersensitivity is part of the diagnostic criteria for ASD, and the results of our stratified analysis suggest that ASD symptoms may contribute to increased perceptual sensitivity in children with ADHD. ASD symptoms did not appear to contribute to pain sensitivity. The results of this stratified analysis were close enough to our original results to suggest that the associations we observed are generalizable to children with ADHD regardless of ASD symptoms [31]. In our sample, 36 participants (29%) had clinically relevant ASD symptoms, which is not surprising given the genetic and epidemiological overlap, with half of the children with ASD also having ADHD [80]. Up to 60% of children with ADHD exhibit co-occurring social difficulties, and social difficulties are core features of autism. ASD, ADHD, and sensory over-responsiveness may have similar symptoms and frequently co-occur. Determining which condition or conditions drive symptom presentation is difficult without a clinical evaluation [80–83].

This study has several strengths. The data were from three sites in two countries; thus our findings are more widely generalizable than they would be from a single site alone. The sensitivity analyses, though exploratory, allowed evaluation of possible factors which could have confounded the results. Further, the results survived correction for multiple testing. Study limitations include the use of subjective parent-report questionnaires as outcome measures that may have resulted in reporting bias. Because the data were cross-sectional, we cannot determine a causal relationship between sensory over-responsiveness and emotional dysregulation. Longitudinal studies are needed to examine causality and the progression of these symptoms over time.

Conclusion

Pain sensitivity and perceptual sensitivity were both positively associated with the severity of emotional dysregulation in this study of children with ADHD. Considering these findings, longitudinal studies are warranted to examine the temporal association and direction of possible causality between sensory over responsiveness and emotional dysregulation in ADHD.

Supplementary Material

Supplementary Material

IMPLICATIONS FOR REHABILITATION.

  • Emotional dysregulation and sensory over-responsiveness are both common in children with ADHD and contribute to added challenges in school and family life.

  • Two types of sensory over-responsiveness, pain sensitivity and perceptual sensitivity, were associated with emotional dysregulation in children with ADHD in our study.

  • Sensory over-responsiveness may be a modifiable treatment target.

Funding

Dr. Bruton’s work was supported by Oregon Health & Science University and by grants from NIH (NIH-NCCIH T32 #AT002688). Funding for the MADDY study has come through private donations to the Nutrition and Mental Health Research Fund, managed by the Foundation for Excellence in Mental Health Care (FEMHC), as well as from a direct grant from FEMHC and funding from the Gratis Foundation. Dr. Johnstone received support from NIH-NCCIH 5R90AT00892403 through the National University for Natural Medicine. Dr. Johnstone’s work on study inception and design was funded by NIH-NCCIH T32 AT002688, as well as through support from the Department of Child and Adolescent Psychiatry, Oregon Health & Science University and Oregon Clinical & Translational Research, through the National Center for Advancing Translational Sciences of the National Institutes of Health under award number UL1TR000128. Dr. Leung’s position is supported by the Emmy Droog (endowed) chair in Complementary and Alternative Healthcare. The study at the Canadian site is funded by the Nutrition and Mental Health Research Fund, administered by the Calgary Foundation. The other authors have no funding sources to disclose.

Disclosure statement

Dr. Arnold has received research funding from Curemark, Forest, Lilly, Neuropharm, Novartis, Noven, Otsuka, Roche/Genentech, Shire, Supernus, and YoungLiving (as well as NIH and Autism Speaks), has consulted with CHADD, Neuropharm, Organon, Pfizer, Sigma Tau, Shire, Tris Pharma, and Waypoint, and been on advisory boards for Arbor, Ironshore, Novartis, Noven, Otsuka, Pfizer, Roche, Seaside Therapeutics, Sigma Tau, Shire. The other authors have no conflicts of interest to disclose.

Footnotes

Supplemental data for this article can be accessed here.

References

  • [1].Danielson ML, Bitsko RH, Ghandour RM, et al. Prevalence of parent-reported ADHD diagnosis and associated treatment among U.S. Children and adolescents, 2016. J Clin Child Adolesc Psychol. 2018;47(2):199–212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [2].American Psychiatric Association. DSM-V: diagnostic and statistical manual of mental disorders. Fifth. American Psychiatric Association; 2013. [Google Scholar]
  • [3].Shaw P, Stringaris A, Nigg J, et al. Emotion dysregulation in attention deficit hyperactivity disorder. American Psychiatric Association; 2014;171:276–293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [4].Faraone SV, Rostain AL, Blader J, et al. Practitioner review: Emotional dysregulation in attention-deficit/hyperactivity disorder – implications for clinical recognition and intervention. J Child Psychol Psychiatry. 2019;60(2):133–150. [DOI] [PubMed] [Google Scholar]
  • [5].Riley AW, Spiel G, Coghill D, et al. Factors related to Health-Related quality of life (HRQoL) among children with ADHD in Europe at entry into treatment. Eur Child Adolesc Psychiatry. 2006;15(S1):i38–i45. [DOI] [PubMed] [Google Scholar]
  • [6].Fernández de la Cruz L, Simonoff E, McGough JJ, et al. Treatment of children with attention-deficit/hyperactivity disorder (ADHD) and irritability: results from the multimodal treatment study of children with ADHD (MTA). J Am Acad Child Adolesc Psychiatry. 2015;54(1):62–70.e3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [7].Miller LJ, Anzalone ME, Lane SJ, et al. Concept evolution in sensory integration: a proposed nosology for diagnosis. Am J Occup Ther. 2007;61(2):135–142. [DOI] [PubMed] [Google Scholar]
  • [8].Ahn RR, Miller LJ, Milberger S, et al. Prevalence of parents’ perceptions of sensory processing disorders among kindergarten children. Am J Occup Ther. 2004;58(3):287–293. [DOI] [PubMed] [Google Scholar]
  • [9].Lane SJ, Reynolds S, Thacker L. Sensory over-responsivity and ADHD: differentiating using electrodermal responses, cortisol, and anxiety. Front Integr Neurosci. 2010;4:8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [10].Parush S, Sohmer H, Steinberg A, et al. Somatosensory function in boys with ADHD and tactile defensiveness. Physiol Behav. 2007;90(4):553–558. [DOI] [PubMed] [Google Scholar]
  • [11].Dunn W. The impact of sensory processing abilities on the daily lives of young children and their families: a conceptual model. Infants Young Child. 1997;9(4):23–35. [Google Scholar]
  • [12].Berkowitz L. Pain and aggression: some findings and implications. Motiv Emot. 1993;17(3):277–293. [Google Scholar]
  • [13].Séguin JR, Pihl RO, Boulerice B, et al. Pain sensitivity and stability of physical aggression in boys. J Child Psychol Psychiatry. 1996;37(7):823–834. [DOI] [PubMed] [Google Scholar]
  • [14].Benarous X, Bury V, Lahaye H, et al. Sensory processing difficulties in youths with disruptive mood dysregulation disorder. Front Psychiatry. 2020;11:1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [15].Shimizu VT, Bueno OFA, Miranda MC. Sensory processing abilities of children with ADHD. Braz J Phys Ther. 2014; 18(4):343–352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [16].DeSerisy M, Hirsch E, Roy AK. The contribution of sensory sensitivity to emotional lability in children with ADHD symptoms. Evid Based Pract Child Adolesc Ment Health. 2019;4(4):319–327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [17].Mangeot SD, Miller LJ, McIntosh DN, et al. Sensory modulation dysfunction in children with attention-deficit-hyperactivity disorder. Dev Med Child Neurol. 2001;43(6): 399–406. [DOI] [PubMed] [Google Scholar]
  • [18].Dunn W. The sensations of everyday life: empirical, theoretical, and pragmatic considerations. Am J Occup Ther. 2001; 55(6):608–620. [DOI] [PubMed] [Google Scholar]
  • [19].Fuermaier ABM, Hüpen P, De Vries SM, et al. Perception in attention deficit hyperactivity disorder. Atten Defic Hyperact Disord. 2018;10(1):21–47. [DOI] [PubMed] [Google Scholar]
  • [20].Bar-Shalita T, Granovsky Y, Parush S, et al. Sensory modulation disorder (SMD) and pain: a new perspective. Front Integr Neurosci. 2019;13:27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [21].Tallal P, Miller S, Fitch RH. Neurobiological basis of speech: a case for the preeminence of temporal processing. Ann NY Acad Sci. 1993;682(1):27–47. [DOI] [PubMed] [Google Scholar]
  • [22].Bamiou DE, Musiek FE, Luxon LM. Aetiology and clinical presentations of auditory processing disorders-a review. Arch Dis Child. 2001;85(5):361–365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [23].Reynolds S, Lane SJ. Sensory overresponsivity and anxiety in children with ADHD. Am J Occup Ther. 2009;63(4): 433–440. [DOI] [PubMed] [Google Scholar]
  • [24].Hermesdorf M, Berger K, Baune BT, et al. Pain sensitivity in patients with major depression: differential effect of pain sensitivity measures, somatic cofactors, and disease characteristics. J Pain. 2016;17(5):606–616. [DOI] [PubMed] [Google Scholar]
  • [25].Sharma S, Ohrbach R, Fillingim RB, et al. Pain sensitivity modifies risk of injury-related temporomandibular disorder. J Dent Res. 2020;99(5):530–536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [26].Johnstone JM, Leung B, Gracious B, et al. Rationale and design of an international randomized placebo-controlled trial of a 36-ingredient micronutrient supplement for children with ADHD and irritable mood: the micronutrients for ADHD in youth (MADDY) study. Contemp Clin Trials Commun. 2019;16:100478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [27].Johnstone JM, Hatsu I, Tost G, et al. Micronutrients for attention-deficit/hyperactivity disorder in youths: a placebo-controlled randomized clinical trial. J Am Acad Child Adolesc Psychiatry. 2021:S0890–8567(21)00473–1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [28].Rucklidge JJ, Eggleston MJF, Johnstone JM, et al. Vitamin-mineral treatment improves aggression and emotional regulation in children with ADHD: a fully blinded, randomized, placebo-controlled trial. J Child Psychol Psychiatry. 2018;59(3):232–246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [29].M H, A B, T B, et al. Psychometric validity of the strengths and difficulties questionnaire-dysregulation profile. Psychopathology. 2011;44(1):53–59. [DOI] [PubMed] [Google Scholar]
  • [30].Deutz MHF, Shi Q, Vossen HGM, et al. Evaluation of the strengths and difficulties Questionnaire-Dysregulation Profile (SDQ-DP)). Psychol Assess. 2018;30(9):1174–1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [31].Gadow K, Sprafkin J. Child & adolescent symptom inventory-5. 5th ed. 2013. Stonybrook (NY): Checkmate Plus; 2013. [Google Scholar]
  • [32].Gadow KD, Sprafkin J. The symptom inventories: an annotated bibliography. Stony Brook (NY): Checkmate Plus; 2015. [Google Scholar]
  • [33].Johnstone JM, Leung BMY, Srikanth P, et al. Development of a composite primary outcome score for children with Attention-Deficit/hyperactivity disorder and emotional dysregulation. J Child Adolesc Psychopharmacol. 2020;30(3): 166–172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [34].Simonds J, Rothbart MK. The Temperament in Middle Childhood Questionnaire (TMCQ): A Computerized Self-Report Instrument for Ages 7–10. In: Occasional Temperament Conference, Athens, GA. 2004. [Google Scholar]
  • [35].Nigg JT, Antovich D, Karalunas SL. Temperament in middle childhood questionnaire: new data on factor structure and applicability in child clinical sample [under review]. Portland, OR; 2020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [36].Boyd R, Lindo E, Weeks L, et al. On Racism: A New Standard For Publishing On Racial Health Inequities | Health Affairs. 2020. [cited 2020 Dec 1]. Available from: https://www.healthaffairs.org/do/10.1377/hblog20200630.939347/full/.
  • [37].Winthorst WH, Bos EH, Roest AM, et al. Seasonality of mood and affect in a large general population sample. PLOS One. 2020;15(9):e0239033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [38].VanderWeele TJ. Principles of confounder selection. Eur J Epidemiol. 2019;34(3):211–219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [39].Stodden V, McNutt M, Bailey DH, et al. Enhancing reproducibility for computational methods. American Association for the Advancement of Science. 2016;354(6317): 1240–1241. [DOI] [PubMed] [Google Scholar]
  • [40].Ernst AF, Albers CJ. Regression assumptions in clinical psychology research practice-a systematic review of common misconceptions. PeerJ. 2017;5(5):e3323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [41].Fox J. Applied regression analysis and generalized linear models. 3rd ed. McMaster Univeristy. Canada: Sage Publications; 2015. [Google Scholar]
  • [42].Hayes AF, Cai L. Using heteroskedasticity-consistent standard error estimators in OLS regression: an introduction and software implementation. Behav Res Methods. 2007;39(4): 709–722. [DOI] [PubMed] [Google Scholar]
  • [43].Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57(1):289–300. [Google Scholar]
  • [44].Kaat AJ, Gadow KD, Lecavalier L. Psychiatric symptom impairment in children with autism spectrum disorders. J Abnorm Child Psychol. 2013;41(6):959–969. [DOI] [PubMed] [Google Scholar]
  • [45].von Elm E, Altman DG, Egger M, et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med. 2007;147(8):573–577. [DOI] [PubMed] [Google Scholar]
  • [46].Bruton A, Leung B, Hatsu I, et al. Does sensory modulation dysfunction contribute to emotional dysregulation in children with ADHD? Analysis plan. medRxiv. 2020. [Google Scholar]
  • [47].StataCorp. Stata statistical software. College Station (TX): StataCorp LLC; 2019. [Google Scholar]
  • [48].Northover C, Thapar A, Langley K, et al. Pain sensitivity in adolescent males with Attention-Deficit/hyperactivity disorder: testing for associations with conduct disorder and callous and unemotional traits. PLOS One. 2015;10(7): e0134417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [49].McIntosh DN, Miller LJ, Shyu V, et al. Development and validation of the short sensory profile. 1999. [cited 2021 Sep 30]. p. 59–73. Available from: https://scholar.google.com/scholar_lookup?journal=Sensory+Profile+User’sManual&title=Development+and+validation+of+theshort+sensory+-profile&author=DN+McIntosh&author=LJ+Miller&author=V+Shyu&author=W+Dunn&publication_year=1999&pages=59-73&.
  • [50].Achenbach TM. Child behavior checklist. In: Encyclopedia of clinical neuropsychology. New York: Springer; 2011. [Google Scholar]
  • [51].Dunn W. Sensory profile. San Antonio, Texas: Scientific Research Publishing; 1999. [Google Scholar]
  • [52].Achenbach TM. Manual for The Child Behavior Checklist/4–18 and 1991 Profile. Univ Vermont, Dep Psychiatry. 1991. [cited 2021 Nov 17]; Available from: https://ci.nii.ac.jp/naid/20001666977. [Google Scholar]
  • [53].Shields A, Cicchetti D. Emotion regulation among school-age children: the development and validation of a new criterion Q-sort scale. Dev Psychol. 1997;33(6):906–916. [DOI] [PubMed] [Google Scholar]
  • [54].Brown C, Tollefson N, Dunn W, et al. The adult sensory profile: measuring patterns of sensory processing. Am J Occup Ther. 2001;55(1):75–82. [DOI] [PubMed] [Google Scholar]
  • [55].Schoen S. Pilot Study of the Sensory Over-Responsivity Scales: Assessment and Inventory DSM-5 SPD Proposal View project Integrated Listening Systems for Children with Sensory Problems View project. 2008. [cited 2021 Feb 10]; Available from: https://www.researchgate.net/publication/23179300.
  • [56].Tavassoli T, Hoekstra RA, Baron-Cohen S. The sensory perception quotient (SPQ): development and validation of a new sensory questionnaire for adults with and without autism. Mol Autism. 2014;5(1):29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [57].Bröring T, Rommelse N, Sergeant J, et al. Sex differences in tactile defensiveness in children with ADHD and their siblings. Dev Med Child Neurol. 2008;50(2):129–133. [DOI] [PubMed] [Google Scholar]
  • [58].Ghanizadeh A. Tactile sensory dysfunction in children with ADHD. Behav Neurol. 2008;20(3):107–112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [59].Lane SJ, Reynolds S. Sensory over-responsivity as an added dimension in ADHD. Front Integr Neurosci. 2019;13:40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [60].Adra N, Cao A, Makris N, et al. Sensory modulation disorder and its neural circuitry in adults with ADHD: a pilot study. Brain Imaging Behav. 2021;15(2):930–940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [61].Ghanizadeh A. Sensory processing problems in children with ADHD, a systematic review. Korean Neuropsychiatric Association. 2011;8:89–94. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [62].Aron EN, Aron A. Sensory-processing sensitivity and its relation to introversion and emotionality. J Pers Soc Psychol. 1997;73(2):345–368. [DOI] [PubMed] [Google Scholar]
  • [63].Bijlenga D, Tjon-Ka-Jie JYM, Schuijers F, et al. Atypical sensory profiles as core features of adult ADHD, irrespective of autistic symptoms. Eur Psychiatry. 2017;43:51–57. [DOI] [PubMed] [Google Scholar]
  • [64].Pluess M, Boniwell I. Sensory-Processing sensitivity predicts treatment response to a school-based depression prevention program: evidence of vantage sensitivity. Pers Individ Dif. 2015;82:40–45. [Google Scholar]
  • [65].McIntosh DN, Miller LJ, Shyu V, et al. Sensory-modulation disruption, electrodermal responses, and functional behaviors. Dev Med Child Neurol. 2007;41(9):608–615. [DOI] [PubMed] [Google Scholar]
  • [66].Schaaf RC, Miller LJ, Seawell D, et al. Children with disturbances in sensory processing: a pilot study examining the role of the parasympathetic nervous system. Am J Occup Ther. 2003;57(4):442–449. [DOI] [PubMed] [Google Scholar]
  • [67].Bar-Shalita T, Vatine JJ, Seltzer Z, et al. Psychophysical correlates in children with sensory modulation disorder (SMD). Physiol Behav. 2009;98(5):631–639. [DOI] [PubMed] [Google Scholar]
  • [68].Bar-Shalita T, Vatine JJ, Parush S, et al. Psychophysical correlates in adults with sensory modulation disorder. Disabil Rehabil. 2012;34(11):943–950. [DOI] [PubMed] [Google Scholar]
  • [69].Weissman-Fogel I, Granovsky Y, Bar-Shalita T. Sensory over-responsiveness among healthy subjects is associated with a pronociceptive state. Pain Pract. 2018;18(4):473–486. [DOI] [PubMed] [Google Scholar]
  • [70].Owen JP, Marco EJ, Desai S, et al. Abnormal white matter microstructure in children with sensory processing disorders. NeuroImage Clin. 2013;2(1):844–853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [71].Ayres J. Sensory integration and learning disorders. Los Angeles (CA): Western Psychological Services; 1972. [Google Scholar]
  • [72].May-Benson TA, Koomar JA. Systematic review of the research evidence examining the effectiveness of interventions using a sensory integrative approach for children. AJOT Am J Occup Ther. 2010;64(3):403–415. [DOI] [PubMed] [Google Scholar]
  • [73].Miller LJ, Coll JR, Schoen SA. A randomized controlled pilot study of the effectiveness of occupational therapy for children with sensory modulation disorder. Am J Occup Ther. 2007;61(2):228–238. [DOI] [PubMed] [Google Scholar]
  • [74].Case-Smith J, Bryan T. The effects of occupational therapy with sensory integration emphasis on preschool-age children with autism. Am J Occup Ther. 1999;53(5):489–497. [DOI] [PubMed] [Google Scholar]
  • [75].Linderman TM, Stewart KB. Sensory integrative-based occupational therapy and functional outcomes in young children with pervasive developmental disorders: a single-subject study. Am J Occup Ther. 1999;53(2):207–213. [DOI] [PubMed] [Google Scholar]
  • [76].Schroeder RH. Improvement in academic achievement through enhancement of perceptual and sensory integrative functioning. School Psychol Int. 3(2):97–103. [Google Scholar]
  • [77].Miller LJ, Schoen SA, James K, et al. Lessons learned: a pilot study on occupational therapy effectiveness for children with sensory modulation disorder. Am J Occup Ther. 2007; 61(2):161–169. [DOI] [PubMed] [Google Scholar]
  • [78].Schaaf RC, Benevides T, Mailloux Z, et al. An intervention for sensory difficulties in children with autism: a randomized trial. J Autism Dev Disord. 2014;44(7): 1493–1506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [79].Scanlan JN, Novak T. Sensory approaches in mental health: a scoping review. Aust Occup Ther J. 2015;62(5):277–285. [DOI] [PubMed] [Google Scholar]
  • [80].Zablotsky B, Bramlett MD, Blumberg SJ. The co-occurrence of autism spectrum disorder in children with ADHD. J Atten Disord. 2020;24(1):94–103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [81].Mulligan A, Anney RJL, O’Regan M, et al. Autism symptoms in Attention-Deficit/hyperactivity disorder: a familial trait which correlates with conduct, oppositional defiant, language and motor disorders. J Autism Dev Disord. 2009; 39(2):197–209. [DOI] [PubMed] [Google Scholar]
  • [82].Grzadzinski R, Di Martino A, Brady E, et al. Examining autistic traits in children with ADHD: does the autism spectrum extend to ADHD? J Autism Dev Disord. 2011;41(9): 1178–1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [83].Leitner Y. The co-occurrence of autism and attention deficit hyperactivity disorder in children – what do we know? Front Hum Neurosci. 2014;8:268. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Material
NIHMS1789129-supplement-Supplementary_Material.docx (7.3MB, docx)

RESOURCES