RESEARCH ARTICLE Investigating Interoception and Body Awareness in Adults With and Without Autism Spectrum Disorder Lisa Fiene and Charlotte Brownlow This study aimed to investigate the current gap in the literature with regard to how adults with and without Autism Spectrum Disorder (ASD) interpret elements of the interoceptive sense, which includes thirst, hunger, temperature, satiety, and the prediction of onset of illness. Adults with a diagnosed ASD (n 5 74; 36 males, 38 females) were compared to a control group (n 5 228; 53 males, 174 females, 1 unspecified) in their self-reported perceptions of body awareness utilizing the Body Awareness Questionnaire (BAQ) and thirst awareness using the Thirst Awareness Scale (TAS). Those in the ASD group reported a clinically significant lower body and thirst awareness compared to the control group, and this was a large effect (BAQ; d 5 21.26, P < 0.001; TAS; d 5 21.02, P < 0.001). These findings are of clinical importance, as difficulty with sensing internal bodily states could theoretically impact on the physical and C 2015 mental health, social interactions and self-awareness of adults with ASD. Autism Res 2015, 8: 709–716. V International Society for Autism Research, Wiley Periodicals, Inc. Keywords: Autism; Asperger’s syndrome; interoception; body awareness; ASD; thirst; hunger; temperature
Introduction The diagnosis of Autism Spectrum Disorder (ASD) has increased dramatically over the last few decades, with current prevalence estimates indicating that an average of 1 in 68 people in the western world are on the spectrum [Baron-Cohen et al., 2009; Centers for Disease Control & Prevention, 2014]. Global estimates are lower at an average of 1 in162, however researchers postulate this may be owing to different methodological and cultural approaches [Barnevik-Olsson, Gillberg, & Fernell, 2008; Elsabbagh et al., 2012; Wong & Hui, 2008]. Males are more likely to be diagnosed, with the ratio of males to females being reported to be anywhere between 46:1 [Lai, Tseng, Hou, & Guo, 2012; Rivet & Matson, 2011]. ASD is a complex heterogeneous neurodevelopmental disorder, resulting from underlying dysfunctions in the central nervous system, and current research is focused on a neurobiological approach to understanding its aetiology [Matson & Neal, 2009; Stigler, McDonald, Anand, Saykin, & McDougle, 2011]. In the latest Diagnostic and Statistical Manual of Mental Disorders [5th ed.; DSM-5; American Psychiatric Association, 2013], the triad impairments of social interaction, communication, restrictive and repetitive behaviors have been condensed into a dyad of two domains: social communication domain and fixated interests and
repetitive behavior domain. Previously, ASD was considered an umbrella term, incorporating Autistic Disorder, Asperger’s Syndrome, and Pervasive Developmental Disorder–Not Otherwise Specified (PDD-NOS), however these separate diagnoses have been subsumed into the single diagnosis of ASD, where individuals can present anywhere on the spectrum of each limitation and its sub-criteria [Matson, Hattier, & Williams, 2012]. Sensory perception abnormalities have also been incorporated in the diagnosis, as individuals with ASD often have interrupted or inaccurate sensory processing abilities [Bogdashina, 2003; Crane, Goddard, & Pring, € der, & Kjellin, 2012; Kern et al., 2009; Elwin, Ek, Schro 2006]. Current research has found that these abnormalities can either be hyperreactivity or hyporeactivity to stimuli, or a combination of both, and these can lead to unusual behaviors [Lane, Young, Baker, & Angley, 2010]. Hyperreactivity is a high sensitivity to stimulation, whereas hyporeactivity is a low or diminished sensitivity to stimulation. For example, individuals with a hyperreactivity to sounds may avoid sounds and noises, make repetitive noises to block out other sounds and cover their ears, while those who are hyporeactive to visual stimuli may be fascinated with reflections and bright colored objects and move fingers or objects in front of the eyes [Bogdashina, 2003; Lane et al., 2010]. Existing research, however, has mainly
From the School of Psychology and Counselling, University of Southern Queensland, Toowoomba, Queensland, 4350, Australia Received May 12, 2014; accepted for publication March 02, 2015 Address for correspondence and reprints: Charlotte Brownlow, School of Psychology and Counselling, University of Southern Queensland, Toowoomba, Queensland 4350, Australia. E-mail: [email protected] Published online 25 March 2015 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/aur.1486 C 2015 International Society for Autism Research, Wiley Periodicals, Inc. V
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Autism Research 8: 709–716, 2015
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focused on how people with ASD process external stimuli, which include sights and sounds etc., with the notable exception of Elwin et al. [2012] who conducted a qualitative study to investigate the individual reactions to both internal and external stimuli. At the time of this writing however, no quantitative studies could be found of how people with ASD interpret internal stimuli, the sense of the physiological condition of the body. This sense, called interoception or body awareness, is a homeostatic system which relates back to the individual their subjective well-being, their “material me.” It includes the highly resolved feelings of thirst, hunger, temperature, satiety, heartbeat, air hunger, pain, itch, CT affective touch, gustation, vasomotor activity, muscular and visceral sensations [Craig, 2003]. The general consensus is that interoception is an afferent pathway, where signals are conveyed back on the status of all tissues of the body, via the Lamina I neurons in the spinal cord [Craig, 2009; Menon & Uddin, 2010]. Together with afferents that are relayed by the Nucleus of the Solitary Tract (NTS), a direct thalamocortical representation of the physiological state of the body is generated [Craig, 2002]. One model states that a “salience” network then identifies what is most relevant among several stimuli to guide behavior [Uddin & Menon, 2009]. This salience network involves key nodes in the Anterior Insula (AI) and the Anterior Cingulate Cortex, where the AI is the network hub, providing an alert signal to initiate brain responses to salient stimuli. This is expressed as a dominant feeling state that Menon and Uddin [2010] found to be a modulator for social and motivational behavior in combination with homeostasis. Researchers hypothesized that ineffective salience processing in the AI may be a hallmark of Autism, as lowered activity levels in the AI have been found [Di Martino et al., 2009; Menon & Uddin, 2010; Uddin & Menon, 2009]. This hypoactivity may be evidenced as a sensory agnosia of internal bodily states. The investigation of interoceptive awareness in ASD populations, compared to a control group, is therefore warranted to test this hypothesis. Fair-Field [2012] postulated that inaccurate interoceptive abilities may lead to the inability to appropriately recognize and respond to sensations of hunger, thirst, temperature, and satiety etc. For example, this may present as excessive fluid drinking behaviors and water intoxication, which has been observed in individuals with ASD [Terai, Munesue, & Hiratani, 1999]. As water intoxication can also lead to seizures [Verbalis, 2010], further research to explore this relationship was recommended, as epilepsy co-occurs in approximately 30% of individuals diagnosed with ASD [Hiratani, Munesue, Terai, & Haruki, 1997; Mouridsen, Rich, & Isager, 2011; Spence & Schneider, 2009; Terai et al., 1999].
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To assess elements of interoceptive awareness, specifically thirst, hunger, temperature, satiety and the prediction of the onset of illness, the Body Awareness Questionnaire (BAQ), and Thirst Awareness Scale (TAS) were used for the purposes of this study. The TAS was created by the authors of this research, as thirst/satiety awareness is not included in the BAQ and yet is an important aspect of the interoceptive sense [Craig, 2003]. First, it was anticipated that there would be differences between adults with and without ASD in their selfreported BAQ scores. Second, it was proposed that there would be differences between the two groups in their self-reported TAS scores. Third, it was proposed that there would be differences between the two groups in the relationship between their self-reported TAS scores and fluid drinking behaviors. As previous research had found that females were more likely to report higher body awareness than males in people without ASD [Shields, Mallory, & Simon, 1989], a two way ANOVA was also undertaken with gender and group as the independent variables.
Method Participants The control sample consisted of 228 survey participants (53 males, 174 females, 1 unspecified) undergraduate psychology students, with age ranges from 17 to 67 years (Mage 5 31.53, SD 5 11.93 years). The ASD sample consisted of 74 survey participants (36 males, 38 females), with age ranges from 18 to 65 years (Mage 5 36.73, SD 5 12.52). Participants in the ASD group were required to meet the selection criteria of being over 18 years of age, and had previously been diagnosed with an ASD by an appropriately qualified professional (Autistic Disorder, n 5 6, Asperger’s Syndrome, n 5 65, PDD-NOS, n 5 3). The rationale for identifying Autistic Disorder, Asperger’s Syndrome or PDD-NOS was due to participants being diagnosed under a previous DSM, and therefore would have a range of diagnoses and would identify with these diagnoses. Materials Interoception measure. The BAQ [Shields et al., 1989] was used to measure components of interoception as no existing instrument could be found that measured interoception in its entirety. The 18-item selfreport BAQ, however, is a reliable and valid instrument for measuring the ability to identify inner sensations and to discern the subtle homeostatic bodily cues that alert to varying functional states of the body. As the BAQ has not yet been utilized in ASD populations, reliability measures comparing the results of those with and without ASD were included in the analysis.
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Multiple studies have found that the BAQ possesses good reliability (a 5 0.83), as well as acceptable convergent and discriminant validity [Mehling et al., 2009; Shields et al., 1989]. The BAQ is a Likert scale, where participants report on a scale from 1 “Not at all true of me” to 7 “Very true of me” their answers to items such as “I can always tell when I bump myself whether or not it will become a bruise,” “I notice specific bodily reactions to being overhungry,” “I know I’m running a fever without taking my temperature,” “I always know when I’ve exerted myself to the point where I’ll be sore the next day,” and “I can distinguish between tiredness because of hunger and tiredness because of lack of sleep.” One negatively worded item “I don’t notice seasonal rhythms and cycles in the way my body functions” was reverse scored. A higher total BAQ score, therefore, indicated a greater level of awareness of these body processes.
Thirst awareness measure. As no existing instrument could be found which measured interoceptive thirst awareness, the TAS was developed by the researchers for the purposes of this study. This scale was a self-report measure of thirst identification and liquid consumption. The initial item pool consisted of nine items, which measured the construct of awareness of the thirst/satiety response. Items such as “I notice distinct body reactions when I am thirsty” and “I notice specific body reactions when I am no longer thirsty” were asked on a 7-point Likert-type scale, where 1 represented “Not at all true of me” through to 7 “Very true of me.” A higher TAS score therefore indicated a greater awareness of the sensation of thirst/satiety. As the scale was in its development, preliminary factor, reliability and validity analyses were also undertaken as part of this study. Procedure Ethics approval for this study was granted prior to commencement from a university Human Research Ethics Committee. Convenience sampling was utilized for both groups, with participants voluntarily completing an anonymous online survey, which included nonidentifiable demographic questions and online versions of the BAQ and TAS. Questions relating to the average amount of nonalcoholic fluids consumed per day and numbers of seizures experienced were also asked. Research has found that self-report of nonalcoholic beverage intake represents an adequate assessment tool, with acceptable reliability and validity [Nelson & Lytle, 2009]. Those in the ASD group voluntarily responded to online links to the survey which were listed on a range of ASD websites, forums, and newsletters, with no
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incentives offered. Gatekeeper approvals were obtained from all ASD websites, forums, and newsletters prior to the survey being advertized. Informed consent for all participants was completed after information on the study was provided, with participants being advised that participation was entirely voluntary and they could withdraw at any time without penalty. Feedback on the overall results was also available on request. Those without ASD consisted of undergraduate psychology students, with a 1% course credit or entry into the Department of Psychology raffle offered as an incentive for participation. Data were analyzed using SPSS 21.0 and Exploratory Software for Confidence Intervals [Cumming, 2011]. An a priori power analysis using G*Power 3.1.5 [Faul, Erdfelder, Buchner, & Lang, 2009] was conducted (f2 5 0.25, a 5 0.05), where to detect a medium effect with a power of 0.80 a minimum sample size of 225 was required. As the total sample size was 302, this was deemed adequate for the analyses. Initial data screening revealed that there were no missing values, out of range data or univariate outliers. To minimize Type 1 error, the more conservative Welch’s t-test was applied to all comparisons of independent group means, as equal variances are not assumed and the test corrects for unequal sample sizes [Field, 2009].
Results BAQ Analysis The assumption of normality for both groups was met, however the variances were significantly different in the two groups, F(1, 300) 5 7.34, P 5 0.007. As the sample sizes were quite large however, Hartley’s variance ratio (Fmax) was also reported, as recommended by Field [2009]. The means, standard deviations, confidence intervals, and reliability coefficients of BAQ scores for each group by gender are presented in Table 1. A two way ANOVA was initially conducted with group and gender as the independent variables. Results showed that there was a main effect for group, F(1,300) 5 85.29, P < 0.001, but no main effect for gender, F(1,300) 5 .277, P 5 0.59. There were also no interaction effects, indicating that the magnitude of difference in BAQ scores between males and females across both groups was equal F(1,300) 5 2.29, P 5 0.13. Indeed, the group classification of with or without ASD was found to be the significant variable influencing mean BAQ scores in the present study. Independent-samples Welch’s t-test revealed that there was a statistically significant difference between the mean BAQ scores for the ASD group (M 5 62.16, SD 5 22.52), compared to the group without ASD
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Table 1. Means, 95% Confidence Intervals, Standard Deviations, and Reliability Coefficients of BAQ Scores for Control Group and ASD Group, by Gender Group
Gender
M
Control
Male Female
87.57 84.98 85.59 58.94 64.76 62.16
Total Controla ASD
Male Female
Total ASDb
CI
SD
[83.35,87.84]
[56.94,67.38]
17.27 17.25 17.21 22.86 22.33 22.52
a
0.90
0.90
Note. CI 5 95% confidence interval. n 5 228. b n 5 74. a
(M 5 85.59, SD 5 17.21), t(102) 5 8.21, Mdiff 5 223.43, 95% CI [217.77, 229.09], P < 0.001, d 5 21.26, Fmax 5 1.71. Specifically, those in the ASD group reported a significant hyporeactivity in body awareness compared to the group without ASD, and this was a large effect. Mean BAQ scores for the group without ASD in this present study were consistent with prior research, which found that mean BAQ scores ranged from 80.6 to 94.0 [Boyle, Sayers, Jensen, Headley, & Manos, 2004; Shields et al., 1989]. The alpha coefficients for both the group without ASD (a 5 0.90) and the ASD group (a 5 0.90) indicated high internal consistency of results across items for both groups. TAS Refinement To explore whether the underlying factor structure of the nine items of the preliminary TAS scale represented the construct of thirst awareness, an exploratory factor analysis using principal component analysis with oblique rotation was undertaken. As the total sample consisted of 302 participants, this exceeded the minimum participant to item ratio of at least 5:1 recommended for exploratory factor analysis [Gorsuch, 1983]. The inter-item correlation matrix revealed no multicollinearity or singularity between items, with small to moderate correlations found. The Kaiser-Meyer-Olkin
measure of sampling adequacy was 0.69, indicating a medium to good probability of principal component analysis yielding distinct and reliable factors [Field, 2009]. An initial scree plot indicated there were possibly three or four components to extract, with subsequent parallel analysis using syntax provided by O’Connor [2000] identifying three components with Eigenvalues over 1. The first component accounted for 28.27% of the variance, the second for 22.07% and the third 15.69%, with a cumulative percentage of 66.01% for all three components. Applying Promax rotation and retaining items with absolute pattern component loadings greater than 0.40 revealed a clear, simply structured three-component solution, with one observed cross loading. Breakdown of items, pattern coefficients and communalities of the nine items of the preliminary TAS follow in Table 2. Three items depicting excessive thirst represented the first factor, with these items describing a heightened or hyperreactive thirst response. Three items depicting typical thirst awareness represented the second component, with these items describing nonemotive awareness of the thirst/satiety response. Three items depicting lack of thirst represented the third factor. One item in the lack of thirst component “When I see someone else drinking fluids, it reminds me that I need to drink” also cross-loaded onto the excessive thirst component. No significant correlations between components were found. The preliminary alpha coefficient assessing internal consistency for the nine items was very low (a 5 0.54), indicating poor consistency across items. Systematic deletion of poor performing scale items eventually revealed a three-item TAS, with an acceptable alpha coefficient of 0.72 [Field, 2009]. These remaining items related to typical thirst/satiety awareness, in line with the construct of the BAQ: “I notice distinct body reactions when I am thirsty,” “I notice specific body reactions when I am no longer thirsty,” and “I notice specific body reactions when I have drunk too much
Table 2. Summary Items and Factor Loadings from Principal Components Analysis with Promax Rotation for Thirst Awareness Scale (N 5 302) Component Variable TAS08 TAS02 TAS05 TAS06 TAS04 TAS01 TAS03 TAS07 TAS09
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Item Name
1
I seem to want to constantly drink fluids I feel thirsty all the time I never seem to feel “un-thirsty” I notice specific body reactions when I have drunk too much fluid I notice specific body reactions when I am no longer thirsty I notice distinct body reactions when I am thirsty I have to ask myself “Am I thirsty” I never feel thirsty When I see someone else drinking fluids, it reminds me that I need to drink
0.87 0.86 0.80
2
Communality 3
0.86 0.82 0.72
0.48
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0.84 0.72 0.52
0.75 0.78 0.62 0.64 0.66 0.72 0.71 0.59 0.55
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Table 3. Means, 95% Confidence Intervals, Standard Deviations, and Reliability Coefficients of TAS Scores for Control Group and ASD Group, by Gender Group
Gender
M
Control
Male Female
15.09 14.22 14.42 10.08 10.76 10.43
Total Controla ASD Total ASDb
Male Female
CI
[13.95,14.89]
[9.35,11.51]
SD 3.30 3.70 3.62 5.27 4.03 4.65
a
0.67
Discussion 0.68
Note. CI 5 95% confidence interval. n 5 228. b n 5 74. a
fluid.” Correlation between BAQ scores and the refined three-item TAS scores showed a strong positive relationship, indicating adequate concurrent validity, r(300) 5 0.66, P < 0.001. TAS Analysis The assumption of normality was met for both groups, however the assumption of equal variances was not met F(1,295) 5 9.59, P < 0.001. Again, due to the large sample sizes, the Welch’s t-test was reported with the variance ratio [Field, 2009]. The means, standard deviations, confidence intervals, and reliability coefficients of TAS scores for each group by gender are presented in Table 3. As per the BAQ, a two way ANOVA was initially conducted with group and gender as the independent variables. Results showed that there was a main effect for group, F(1,300) 5 60.10, P < 0.001 but no main effect for gender, F(1,300) 5 0.030, P 5 0.86. There were also no interaction effects, indicating that the magnitude of difference in TAS scores between males and females across both groups was equal F(1,300) 5 2.01, P 5 0.16. Indeed, as per the BAQ results, the group classification of with or without ASD was found to be the significant variable influencing mean TAS scores in this present study. Independent-samples Welch’s t-test revealed that there was a statistically significant difference between mean TAS scores for the ASD group (M 5 10.43, SD 5 4.65), and the group without ASD (M 5 14.42, SD 5 3.62), t(103) 5 6.743, Mdiff 5 23.99, 95% CI [22.82, 25.16], P < 0.001, d 5 21.02, Fmax 5 1.66. Specifically, those in the ASD group reported a significant hyporeactivity in thirst/satiety awareness compared to the group without ASD, and this was a large effect. To investigate the relationship between thirst awareness and fluids consumed, a correlational analysis between TAS scores and reported average amount of fluids consumed per day was undertaken. In the group without ASD, a weak positive relationship was found,
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r(226) 5 0.21, P 5 0.002, 95% CI [0.08, 0.33]. Specifically, as TAS scores increased, the average amount of fluids consumed per day also increased. Within the ASD group, however, no relationship was found, r(72) 5 0.09, P 5 0.43, 95% CI [20.14, 0.33].
This study aimed to address the current gap in the literature with regard to how adults with and without ASD interpret elements of the interoceptive sense, and specifically to what extent there may be differences between the two groups in their reported perception of body awareness. If those with ASD have difficulty in perceiving when they are thirsty, hungry, or ill, a better understanding in this regard may help provide improved outcomes for adults with ASD. Strategies could include designing sensory inclusive interventions and self-awareness programmes which may help those with ASD to cope with the stresses of everyday life. The results from the current study provide support for Craig’s characterization of interoception as a distinct sense of the physiological condition of the body. Strong internal consistency across all item responses, for both groups, suggest that perceptions of temperature, thirst, hunger, satiety etc. form together as part of this unique sensory afferent pathway. First, it was anticipated that there would be differences between the two groups in their self-reported BAQ scores, and this was supported. Specifically, those in the ASD group reported a statistically significant hyporeactivity in body awareness compared to the control group, and this was a large effect. The results showed a distinct ASD population, one which consistently reported a low awareness of internal bodily states compared to the control group. Analysis of Variance revealed that mean BAQ scores were not affected by gender in both groups, with females reporting similar body awareness to males. Specifically, males and females in the ASD group reported significantly lower body awareness, compared to controls. This was an unexpected result, as previous research utilizing the BAQ found that females were more likely to report higher body awareness than males in those without ASD [Shields et al., 1989]. Researchers suggested that females may be generally more internally focused and introspective than males, enhancing the ability to detect nonemotive bodily sensations. Subsequent studies utilizing the BAQ, as well as this current study however, have found no difference between males and females in the general perception of body awareness [Baas, Beery, Allen, Wizer, & Wagoner, 2004; Shields & Simon, 1991]. It may be that the original
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results reflected sampling variability rather than a generalized higher body awareness in females. Indeed, other researchers suggest that the interoceptive sense is an “urge for action,” [Jackson, Parkinson, Kim, € ermann, & Eickhoff, 2011], is innate and nonSchu learned, equally present in males and females [McGlone et al., 2012]. It was proposed that there would be differences between the two groups in their self-reported TAS scores, and this was also supported. Specifically, those in the ASD group reported a statistically significant hyporeactivity in thirst/satiety awareness compared to those without ASD, and this was a large effect. Again, this was a distinct ASD population, one which consistently reported a lower awareness of the thirst/satiety response. The TAS was designed as part of this study to measure the construct of nonemotive thirst awareness and satiety, as this is a prominent aspect of the interoceptive sense which is not included in the BAQ. As such, it was important that the refined TAS was able to reliably discern the subtle homeostatic bodily cues that alert to the typical thirst/satiety response, in line with the construct of the BAQ. While the initial factor analysis revealed three components, only the refined three item TAS was deemed to measure this construct. Demographic analysis of the TAS results also revealed that the mean TAS scores were not affected by gender, with females reporting similar thirst awareness/satiety to males. Indeed, the diagnosis of ASD was found to be the overall contributing variable to the differences in mean scores, both for the BAQ and the TAS in this present study. These findings also support the model proposed by Uddin and Menon [2009] where they proposed that those with ASD may have a difficulty in responding to salient interoceptive stimuli, as the AI is pivotal in detecting changes in bodily states. Their model posited that this may be evidenced as a sensory agnosia, or a modality-specific failure of recognition. Previous fMRI studies in adults with ASD have found that one of the areas consistently showing significant hypoactivity is the right AI, compared to controls, and researchers proposed that an appropriate level of AI activity is needed to initiate brain responses to salient stimuli [Di Martino et al., 2009; Menon & Uddin, 2010; Uddin & Menon, 2009]. They suspected that the hypoactivity may be due to a disconnect between the sensory and limbic structures that project to the AI, leading to a reduction in salience detection [Uddin & Menon, 2009]. Whether there is a general sensory agnosia arising from insufficient activation of the AI, however, has not been specifically tested with this study. An alternative framework is that there is a general difficulty for adults with ASD to introspect and focus attention toward the self, and further research is recommended to explore the relationship.
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Also, the results from the current study provided further quantitative support to qualitative studies that found that those with ASD are often unaware of their own body sensations, and for example, do not feel hunger [Bogdashina, 2003; Elwin, et al., 2012]. This study found that interoceptive sensory abnormalities were not reported by adults with ASD as either a hyperreactivity or hyporeactivity (or a combination of both), but a generalized hyporeactivity to internal stimuli. These results are in contrast to previous studies examining external stimuli (sights and sounds etc.), which have found multiple sensory presentations in people with ASD. The results of the current study, at least for the interoceptive sense, however, show a unified low awareness for those on the Autism Spectrum. As there has been very little research on interoception itself, it cannot be assumed that those with ASD process internal information the same way as they process external information. Further research is, therefore, suggested to investigate whether individuals with ASD have different perceptions of internal and external stimuli. It was also anticipated that there would be differences between the two groups in the relationship between self-reported TAS scores and fluid drinking behaviors, and this was partially supported. Correlational analyses between mean TAS scores and average amount of fluids consumed per day revealed that those in the control group showed a significant weak positive relationship between thirst awareness and amount of fluids consumed per day, while those in the ASD group did not show any relationship. Specifically, those in the ASD group were just as likely to consume large amounts of fluid (120 glasses per day) if they reported very low thirst awareness, or very low amounts of fluid (1–3 glasses per day) if they reported higher awareness. Implications and Future Research The results of the current study showed that this is valuable research, and warrants being expanded across domains. Indeed, Keen [2008] noted that disturbances of self-regulatory and homeostatic processes are frequently observed clinically in people with ASD, but as yet has been poorly researched. For example, they suggested that difficulties with hunger and thirst perception would have major implications in the aetiology of some eating disorders, which have been observed in people with ASD [Keen, 2008]. It has been widely reported that children with ASD have unusual eating and drinking behaviors, but the aetiology has been difficult to ascertain. As such, expanding research on interoceptive awareness and functioning is critical to
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extending the understanding of how these physiological processes may be contributing to ASD. A limitation to the current study is that the majority of those in the ASD group reported being diagnosed with Asperger’s Syndrome (n 5 65), which is generally considered to be on the higher functioning end of the Autism Spectrum. Whether the findings can be generalized to the entire ASD population needs to be explored with further research. However, the results of the current study demonstrated that adults with ASD have difficulty with interpreting thirst, hunger, temperature, satiety and the prediction of the onset of illness, compared to a control group. This is an important clinical finding, as difficulties with sensing internal bodily states could theoretically impact on many aspects of a person’s life, including physical and mental health, social interactions, self-awareness, and communication. Based on the findings of this preliminary study, further research is suggested in this regard.
Conclusion This study has found that adults with ASD experience unusual awareness of elements of the interoceptive sense, compared to a control group. While prior research has found that sensory perceptions in people with ASD can either be hyperreactivity or hyporeactivity to external stimuli, or a combination of both, this study has found that adults with ASD reported a unified hyporeactivity to elements of the interoceptive sense, compared to controls. As the DSM-5 includes hyperreactivity or hyporeactivity to sensory input as a subcriterion for diagnosis of ASD, the results of this study are an important clinical finding, both for diagnosis and for the design of interoceptive self-awareness programmes to provide better outcomes for those on the spectrum.
References American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, American Psychiatric Association. Baas, L.S., Beery, T.A., Allen, G., Wizer, M., & Wagoner, L.E. (2004). An exploratory study of body awareness in persons with heart failure treated medically or with transplantation. Journal of Cardiovascular Nursing, 19, 32–40. Barnevik-Olsson, M., Gillberg, C., & Fernell, E. (2008). Prevalence of autism in children born to Somali parents living in Sweden: A brief report. Journal of Developmental Medicine and Child Neurology, 50, 598–601. Baron-Cohen, S., Scott, F.J., Allison, D., Williams, J., Bolton, P., Matthews, F.E., et al. (2009). Prevalence of autismspectrum conditions: UK school-based population study. British Journal of Psychiatry, 194, 500–509.
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Bogdashina, O. (2003). Sensory perceptual issues in autism and Asperger syndrome. New York, NY: Jessica Kingsley Publishers. Boyle, C.A., Sayers, S.P., Jensen, B.E., Headley, S.A., & Manos, T.M. (2004). The effects of yoga training and a single bout of yoga on delayed onset muscle soreness in the lower extremity. Journal of Strength and Conditioning Research, 18(4), 723–729. Centers for Disease Control and Prevention. (2014). Prevalence of Autism Spectrum Disorder among children aged 8 years (Surveillance Summaries No. 63(SS02);1–21). Viewed 4 October 2014, http://www.cdc.gov/mmwr/preview/ mmwrhtml/ss6302a1.htm?s_cid=ss6302a1_w Craig, A.D. (2002). How do you feel? Interoception: The sense of the physiological condition of the body. Nature Reviews Neuroscience, 3, 655–666. Craig, A.D. (2003). Interoception: The sense of the physiological condition of the body. Current Opinion in Neurobiology, 13, 500–505. Craig, A.D. (2009). How do you feel – now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10, 59–70. Crane, L., Goddard, L., & Pring, L. (2009). Sensory processing in adults with autism spectrum disorders. Autism, 13, 215. Cumming, G. (2011). Exploratory software for confidence intervals [Computer software]. Melbourne, Victoria, Australia: Author. Di Martino, A., Ross, K., Uddin, L.Q., Sklar, A.B., Castellanos, F.X., Milham, M.P. (2009). Functional brain correlates of social and non-social processes in autism spectrum disorders: An activation likelihood estimation meta-analysis. Biological Psychiatry, 65, 63–74. Elsabbagh, M., Divan, G., Koh, Y., Shin Kim, Y., Kuachali, S., Marcın, C., et al. (2012). Global prevalence of Autism and other Pervasive Developmental Disorders. Autism Research, 5, 160–179. € der, A., & Kjellin, L. (2012). AutobioElwin, M., Ek, L., Schro graphical accounts of sensing in Asperger syndrome and high-functioning autism. Archives of Psychiatric Nursing, 26, 420–429. Fair-Field, T. (2012). Autism awareness month: Storytelling our way to the interoceptive sense. Viewed 7 February 2013, http://special-ism.com/autism-awareness-month-storytelling-our-way-to-the-interoceptive-sense/ Faul, F., Erdfelder, E., Buchner, A., & Lang, A.G. (2009). G*Power 3.1.5 [Computer Software]. Kiel, Schleswig-Holstein, Germany: Authors. Field, A.P. (2009). Discovering statistics using SPSS (3rd ed.). London, United Kingdom: Sage. Gorsuch, R.L. (1983). Factor analysis (2nd ed.). Hillsdale, NJ: Erlbaum. Hiratani, M., Munesue, T., Terai, K., & Haruki, S. (1997). Two cases of infantile autism with intermittent water intoxication due to compulsive water drinking and episodic release of antidiuretic hormone (SIADH). No To Hattatsu, 29, 367–372. € ermann, M., & Jackson, S.R., Parkinson, A., Kim, S.Y., Schu Eickhoff, S.B. (2011). On the functional anatomy of the urge-for-action. Cognitive Neuroscience, 2, 227–243. Keen, D.V. (2008). Childhood autism, feeding problems and failure to thrive in early infancy. European Child and Adolescent Psychiatry, 17, 209–216.
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Kern, J.K., Trivedi, M.H., Garver, C.R., Grannemann, B.D., Andrews, A.A., Savla, J.S., et al. (2006). The pattern of sensory processing abnormalities in autism. Autism, 10, 480. Lai, D.C., Tseng, Y.C., Hou, Y.M., & Guo, H.R. (2012). Gender and geographic differences in the prevalence of autism spectrum disorders in children: Analysis of data from the national disability register of Taiwan. Research in Developmental Disabilities, 33, 909–915. Lane, A.E., Young, R.L., Baker, A.E., & Angley, M.T. (2010). Sensory processing subtypes in autism: association with adaptive behaviour. Journal of Autism and Developmental Disorders, 40, 112–122. Matson, J.L., & Neal, D. (2009). Seizures and epilepsy and their relationship to Autism Spectrum Disorders. Research in Autism Spectrum Disorders, 3, 999–1005. Matson, J.L., Hattier, M.A., & Williams, L.W. (2012). How does relaxing the algorithm for Autism affect DSM-V prevalence rates? Journal of Autism Developmental Disorders, 42, 1549–1556. McGlone, F., Olausson, H., Boyle, J.A., Jones-Gotman, M., Dancer, C., Guest, S., et al. (2012). Touching and feeling: Differences in pleasant touch processing between glabrous and hairy skin in humans. European Journal of Neuroscience, 35, 1782–1788. Mehling, W.E., Gopisetty, V., Daubenmier, J., Price, C.J., Hecht, F.M., & Stewart, A. (2009). Body awareness: Construct and self-report measures. Plos One, 4, 1–18. Menon, V., & Uddin, L.Q. (2010). Salience, switching, attention and control: a network model of insula function. Brain Structure and Function, 4, 655–672. Mouridsen, S.E., Rich, B., & Isager, T. (2011). Epilepsy and other central nervous system diseases in atypical autism: A case control study. Journal of Neural Transmission, 118, 621–627.
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Nelson, M.C., & Lytle, L.A. (2009). Development and evaluation of a brief screener to estimate fast-food and beverage consumption among adolescents. Journal of the American Dietetic Association, 109, 730–734. O’Connor, B.P. (2000). SPSS and SAS programs for determining the number of components using parallel analysis and Velicer’s MAP test. Behavior Research Methods, Instrumentation, and Computers, 32, 396–402. Rivet, T.T., & Matson, J.L. (2011). Review of gender differences in core symptomology in Autism Spectrum Disorders. Research in Autism Spectrum Disorders, 5, 957–976. Shields, S.A., Mallory, M.E., & Simon, A. (1989). The body awareness questionnaire: Reliability and validity. Journal of Personality Assessment, 53, 802–815. Shields, S.A., & Simon, A. (1991). Is awareness of bodily change in emotion related to awareness of other bodily processes? Journal of Personality Assessment, 57, 96–109. Spence, S.J., & Schneider, M.T. (2009). The role of epilepsy and epileptiform EEGs in Autism Spectrum Disorders. Pediatric Residency, 65, 699–606. Stigler, K.A., McDonald, B.C., Anand, A., Saykin, A.J., & McDougle, C.J. (2011). Structural and functional magnetic resonance imaging of Autism Spectrum Disorders. Brain Research, 1380, 146–161. Terai, K., Munesue, T., & Hiratani, M. (1999). Excessive water drinking behaviour in Autism. Brain and Development, 21, 103–106. Uddin, L.Q., & Menon, V. (2009). The anterior insula in autism: Under-connected and under-examined, Neuroscience and Biobehavioral Reviews, 33, 1198–1203. Verbalis, J.G. (2010). Brain volume regulation in response to changes in osmolality. Neuroscience, 168, 862–870. Wong, V.C., & Hui, S.L. (2008). Epidemiological study of Autism Spectrum Disorder in China. Journal of Child Neurology, 23, 67–72.
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Introduction The diagnosis of Autism Spectrum Disorder (ASD) has increased dramatically over the last few decades, with current prevalence estimates indicating that an average of 1 in 68 people in the western world are on the spectrum [Baron-Cohen et al., 2009; Centers for Disease Control & Prevention, 2014]. Global estimates are lower at an average of 1 in162, however researchers postulate this may be owing to different methodological and cultural approaches [Barnevik-Olsson, Gillberg, & Fernell, 2008; Elsabbagh et al., 2012; Wong & Hui, 2008]. Males are more likely to be diagnosed, with the ratio of males to females being reported to be anywhere between 46:1 [Lai, Tseng, Hou, & Guo, 2012; Rivet & Matson, 2011]. ASD is a complex heterogeneous neurodevelopmental disorder, resulting from underlying dysfunctions in the central nervous system, and current research is focused on a neurobiological approach to understanding its aetiology [Matson & Neal, 2009; Stigler, McDonald, Anand, Saykin, & McDougle, 2011]. In the latest Diagnostic and Statistical Manual of Mental Disorders [5th ed.; DSM-5; American Psychiatric Association, 2013], the triad impairments of social interaction, communication, restrictive and repetitive behaviors have been condensed into a dyad of two domains: social communication domain and fixated interests and
repetitive behavior domain. Previously, ASD was considered an umbrella term, incorporating Autistic Disorder, Asperger’s Syndrome, and Pervasive Developmental Disorder–Not Otherwise Specified (PDD-NOS), however these separate diagnoses have been subsumed into the single diagnosis of ASD, where individuals can present anywhere on the spectrum of each limitation and its sub-criteria [Matson, Hattier, & Williams, 2012]. Sensory perception abnormalities have also been incorporated in the diagnosis, as individuals with ASD often have interrupted or inaccurate sensory processing abilities [Bogdashina, 2003; Crane, Goddard, & Pring, € der, & Kjellin, 2012; Kern et al., 2009; Elwin, Ek, Schro 2006]. Current research has found that these abnormalities can either be hyperreactivity or hyporeactivity to stimuli, or a combination of both, and these can lead to unusual behaviors [Lane, Young, Baker, & Angley, 2010]. Hyperreactivity is a high sensitivity to stimulation, whereas hyporeactivity is a low or diminished sensitivity to stimulation. For example, individuals with a hyperreactivity to sounds may avoid sounds and noises, make repetitive noises to block out other sounds and cover their ears, while those who are hyporeactive to visual stimuli may be fascinated with reflections and bright colored objects and move fingers or objects in front of the eyes [Bogdashina, 2003; Lane et al., 2010]. Existing research, however, has mainly
From the School of Psychology and Counselling, University of Southern Queensland, Toowoomba, Queensland, 4350, Australia Received May 12, 2014; accepted for publication March 02, 2015 Address for correspondence and reprints: Charlotte Brownlow, School of Psychology and Counselling, University of Southern Queensland, Toowoomba, Queensland 4350, Australia. E-mail: [email protected] Published online 25 March 2015 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/aur.1486 C 2015 International Society for Autism Research, Wiley Periodicals, Inc. V
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focused on how people with ASD process external stimuli, which include sights and sounds etc., with the notable exception of Elwin et al. [2012] who conducted a qualitative study to investigate the individual reactions to both internal and external stimuli. At the time of this writing however, no quantitative studies could be found of how people with ASD interpret internal stimuli, the sense of the physiological condition of the body. This sense, called interoception or body awareness, is a homeostatic system which relates back to the individual their subjective well-being, their “material me.” It includes the highly resolved feelings of thirst, hunger, temperature, satiety, heartbeat, air hunger, pain, itch, CT affective touch, gustation, vasomotor activity, muscular and visceral sensations [Craig, 2003]. The general consensus is that interoception is an afferent pathway, where signals are conveyed back on the status of all tissues of the body, via the Lamina I neurons in the spinal cord [Craig, 2009; Menon & Uddin, 2010]. Together with afferents that are relayed by the Nucleus of the Solitary Tract (NTS), a direct thalamocortical representation of the physiological state of the body is generated [Craig, 2002]. One model states that a “salience” network then identifies what is most relevant among several stimuli to guide behavior [Uddin & Menon, 2009]. This salience network involves key nodes in the Anterior Insula (AI) and the Anterior Cingulate Cortex, where the AI is the network hub, providing an alert signal to initiate brain responses to salient stimuli. This is expressed as a dominant feeling state that Menon and Uddin [2010] found to be a modulator for social and motivational behavior in combination with homeostasis. Researchers hypothesized that ineffective salience processing in the AI may be a hallmark of Autism, as lowered activity levels in the AI have been found [Di Martino et al., 2009; Menon & Uddin, 2010; Uddin & Menon, 2009]. This hypoactivity may be evidenced as a sensory agnosia of internal bodily states. The investigation of interoceptive awareness in ASD populations, compared to a control group, is therefore warranted to test this hypothesis. Fair-Field [2012] postulated that inaccurate interoceptive abilities may lead to the inability to appropriately recognize and respond to sensations of hunger, thirst, temperature, and satiety etc. For example, this may present as excessive fluid drinking behaviors and water intoxication, which has been observed in individuals with ASD [Terai, Munesue, & Hiratani, 1999]. As water intoxication can also lead to seizures [Verbalis, 2010], further research to explore this relationship was recommended, as epilepsy co-occurs in approximately 30% of individuals diagnosed with ASD [Hiratani, Munesue, Terai, & Haruki, 1997; Mouridsen, Rich, & Isager, 2011; Spence & Schneider, 2009; Terai et al., 1999].
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To assess elements of interoceptive awareness, specifically thirst, hunger, temperature, satiety and the prediction of the onset of illness, the Body Awareness Questionnaire (BAQ), and Thirst Awareness Scale (TAS) were used for the purposes of this study. The TAS was created by the authors of this research, as thirst/satiety awareness is not included in the BAQ and yet is an important aspect of the interoceptive sense [Craig, 2003]. First, it was anticipated that there would be differences between adults with and without ASD in their selfreported BAQ scores. Second, it was proposed that there would be differences between the two groups in their self-reported TAS scores. Third, it was proposed that there would be differences between the two groups in the relationship between their self-reported TAS scores and fluid drinking behaviors. As previous research had found that females were more likely to report higher body awareness than males in people without ASD [Shields, Mallory, & Simon, 1989], a two way ANOVA was also undertaken with gender and group as the independent variables.
Method Participants The control sample consisted of 228 survey participants (53 males, 174 females, 1 unspecified) undergraduate psychology students, with age ranges from 17 to 67 years (Mage 5 31.53, SD 5 11.93 years). The ASD sample consisted of 74 survey participants (36 males, 38 females), with age ranges from 18 to 65 years (Mage 5 36.73, SD 5 12.52). Participants in the ASD group were required to meet the selection criteria of being over 18 years of age, and had previously been diagnosed with an ASD by an appropriately qualified professional (Autistic Disorder, n 5 6, Asperger’s Syndrome, n 5 65, PDD-NOS, n 5 3). The rationale for identifying Autistic Disorder, Asperger’s Syndrome or PDD-NOS was due to participants being diagnosed under a previous DSM, and therefore would have a range of diagnoses and would identify with these diagnoses. Materials Interoception measure. The BAQ [Shields et al., 1989] was used to measure components of interoception as no existing instrument could be found that measured interoception in its entirety. The 18-item selfreport BAQ, however, is a reliable and valid instrument for measuring the ability to identify inner sensations and to discern the subtle homeostatic bodily cues that alert to varying functional states of the body. As the BAQ has not yet been utilized in ASD populations, reliability measures comparing the results of those with and without ASD were included in the analysis.
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Multiple studies have found that the BAQ possesses good reliability (a 5 0.83), as well as acceptable convergent and discriminant validity [Mehling et al., 2009; Shields et al., 1989]. The BAQ is a Likert scale, where participants report on a scale from 1 “Not at all true of me” to 7 “Very true of me” their answers to items such as “I can always tell when I bump myself whether or not it will become a bruise,” “I notice specific bodily reactions to being overhungry,” “I know I’m running a fever without taking my temperature,” “I always know when I’ve exerted myself to the point where I’ll be sore the next day,” and “I can distinguish between tiredness because of hunger and tiredness because of lack of sleep.” One negatively worded item “I don’t notice seasonal rhythms and cycles in the way my body functions” was reverse scored. A higher total BAQ score, therefore, indicated a greater level of awareness of these body processes.
Thirst awareness measure. As no existing instrument could be found which measured interoceptive thirst awareness, the TAS was developed by the researchers for the purposes of this study. This scale was a self-report measure of thirst identification and liquid consumption. The initial item pool consisted of nine items, which measured the construct of awareness of the thirst/satiety response. Items such as “I notice distinct body reactions when I am thirsty” and “I notice specific body reactions when I am no longer thirsty” were asked on a 7-point Likert-type scale, where 1 represented “Not at all true of me” through to 7 “Very true of me.” A higher TAS score therefore indicated a greater awareness of the sensation of thirst/satiety. As the scale was in its development, preliminary factor, reliability and validity analyses were also undertaken as part of this study. Procedure Ethics approval for this study was granted prior to commencement from a university Human Research Ethics Committee. Convenience sampling was utilized for both groups, with participants voluntarily completing an anonymous online survey, which included nonidentifiable demographic questions and online versions of the BAQ and TAS. Questions relating to the average amount of nonalcoholic fluids consumed per day and numbers of seizures experienced were also asked. Research has found that self-report of nonalcoholic beverage intake represents an adequate assessment tool, with acceptable reliability and validity [Nelson & Lytle, 2009]. Those in the ASD group voluntarily responded to online links to the survey which were listed on a range of ASD websites, forums, and newsletters, with no
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incentives offered. Gatekeeper approvals were obtained from all ASD websites, forums, and newsletters prior to the survey being advertized. Informed consent for all participants was completed after information on the study was provided, with participants being advised that participation was entirely voluntary and they could withdraw at any time without penalty. Feedback on the overall results was also available on request. Those without ASD consisted of undergraduate psychology students, with a 1% course credit or entry into the Department of Psychology raffle offered as an incentive for participation. Data were analyzed using SPSS 21.0 and Exploratory Software for Confidence Intervals [Cumming, 2011]. An a priori power analysis using G*Power 3.1.5 [Faul, Erdfelder, Buchner, & Lang, 2009] was conducted (f2 5 0.25, a 5 0.05), where to detect a medium effect with a power of 0.80 a minimum sample size of 225 was required. As the total sample size was 302, this was deemed adequate for the analyses. Initial data screening revealed that there were no missing values, out of range data or univariate outliers. To minimize Type 1 error, the more conservative Welch’s t-test was applied to all comparisons of independent group means, as equal variances are not assumed and the test corrects for unequal sample sizes [Field, 2009].
Results BAQ Analysis The assumption of normality for both groups was met, however the variances were significantly different in the two groups, F(1, 300) 5 7.34, P 5 0.007. As the sample sizes were quite large however, Hartley’s variance ratio (Fmax) was also reported, as recommended by Field [2009]. The means, standard deviations, confidence intervals, and reliability coefficients of BAQ scores for each group by gender are presented in Table 1. A two way ANOVA was initially conducted with group and gender as the independent variables. Results showed that there was a main effect for group, F(1,300) 5 85.29, P < 0.001, but no main effect for gender, F(1,300) 5 .277, P 5 0.59. There were also no interaction effects, indicating that the magnitude of difference in BAQ scores between males and females across both groups was equal F(1,300) 5 2.29, P 5 0.13. Indeed, the group classification of with or without ASD was found to be the significant variable influencing mean BAQ scores in the present study. Independent-samples Welch’s t-test revealed that there was a statistically significant difference between the mean BAQ scores for the ASD group (M 5 62.16, SD 5 22.52), compared to the group without ASD
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Table 1. Means, 95% Confidence Intervals, Standard Deviations, and Reliability Coefficients of BAQ Scores for Control Group and ASD Group, by Gender Group
Gender
M
Control
Male Female
87.57 84.98 85.59 58.94 64.76 62.16
Total Controla ASD
Male Female
Total ASDb
CI
SD
[83.35,87.84]
[56.94,67.38]
17.27 17.25 17.21 22.86 22.33 22.52
a
0.90
0.90
Note. CI 5 95% confidence interval. n 5 228. b n 5 74. a
(M 5 85.59, SD 5 17.21), t(102) 5 8.21, Mdiff 5 223.43, 95% CI [217.77, 229.09], P < 0.001, d 5 21.26, Fmax 5 1.71. Specifically, those in the ASD group reported a significant hyporeactivity in body awareness compared to the group without ASD, and this was a large effect. Mean BAQ scores for the group without ASD in this present study were consistent with prior research, which found that mean BAQ scores ranged from 80.6 to 94.0 [Boyle, Sayers, Jensen, Headley, & Manos, 2004; Shields et al., 1989]. The alpha coefficients for both the group without ASD (a 5 0.90) and the ASD group (a 5 0.90) indicated high internal consistency of results across items for both groups. TAS Refinement To explore whether the underlying factor structure of the nine items of the preliminary TAS scale represented the construct of thirst awareness, an exploratory factor analysis using principal component analysis with oblique rotation was undertaken. As the total sample consisted of 302 participants, this exceeded the minimum participant to item ratio of at least 5:1 recommended for exploratory factor analysis [Gorsuch, 1983]. The inter-item correlation matrix revealed no multicollinearity or singularity between items, with small to moderate correlations found. The Kaiser-Meyer-Olkin
measure of sampling adequacy was 0.69, indicating a medium to good probability of principal component analysis yielding distinct and reliable factors [Field, 2009]. An initial scree plot indicated there were possibly three or four components to extract, with subsequent parallel analysis using syntax provided by O’Connor [2000] identifying three components with Eigenvalues over 1. The first component accounted for 28.27% of the variance, the second for 22.07% and the third 15.69%, with a cumulative percentage of 66.01% for all three components. Applying Promax rotation and retaining items with absolute pattern component loadings greater than 0.40 revealed a clear, simply structured three-component solution, with one observed cross loading. Breakdown of items, pattern coefficients and communalities of the nine items of the preliminary TAS follow in Table 2. Three items depicting excessive thirst represented the first factor, with these items describing a heightened or hyperreactive thirst response. Three items depicting typical thirst awareness represented the second component, with these items describing nonemotive awareness of the thirst/satiety response. Three items depicting lack of thirst represented the third factor. One item in the lack of thirst component “When I see someone else drinking fluids, it reminds me that I need to drink” also cross-loaded onto the excessive thirst component. No significant correlations between components were found. The preliminary alpha coefficient assessing internal consistency for the nine items was very low (a 5 0.54), indicating poor consistency across items. Systematic deletion of poor performing scale items eventually revealed a three-item TAS, with an acceptable alpha coefficient of 0.72 [Field, 2009]. These remaining items related to typical thirst/satiety awareness, in line with the construct of the BAQ: “I notice distinct body reactions when I am thirsty,” “I notice specific body reactions when I am no longer thirsty,” and “I notice specific body reactions when I have drunk too much
Table 2. Summary Items and Factor Loadings from Principal Components Analysis with Promax Rotation for Thirst Awareness Scale (N 5 302) Component Variable TAS08 TAS02 TAS05 TAS06 TAS04 TAS01 TAS03 TAS07 TAS09
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Item Name
1
I seem to want to constantly drink fluids I feel thirsty all the time I never seem to feel “un-thirsty” I notice specific body reactions when I have drunk too much fluid I notice specific body reactions when I am no longer thirsty I notice distinct body reactions when I am thirsty I have to ask myself “Am I thirsty” I never feel thirsty When I see someone else drinking fluids, it reminds me that I need to drink
0.87 0.86 0.80
2
Communality 3
0.86 0.82 0.72
0.48
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0.84 0.72 0.52
0.75 0.78 0.62 0.64 0.66 0.72 0.71 0.59 0.55
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Table 3. Means, 95% Confidence Intervals, Standard Deviations, and Reliability Coefficients of TAS Scores for Control Group and ASD Group, by Gender Group
Gender
M
Control
Male Female
15.09 14.22 14.42 10.08 10.76 10.43
Total Controla ASD Total ASDb
Male Female
CI
[13.95,14.89]
[9.35,11.51]
SD 3.30 3.70 3.62 5.27 4.03 4.65
a
0.67
Discussion 0.68
Note. CI 5 95% confidence interval. n 5 228. b n 5 74. a
fluid.” Correlation between BAQ scores and the refined three-item TAS scores showed a strong positive relationship, indicating adequate concurrent validity, r(300) 5 0.66, P < 0.001. TAS Analysis The assumption of normality was met for both groups, however the assumption of equal variances was not met F(1,295) 5 9.59, P < 0.001. Again, due to the large sample sizes, the Welch’s t-test was reported with the variance ratio [Field, 2009]. The means, standard deviations, confidence intervals, and reliability coefficients of TAS scores for each group by gender are presented in Table 3. As per the BAQ, a two way ANOVA was initially conducted with group and gender as the independent variables. Results showed that there was a main effect for group, F(1,300) 5 60.10, P < 0.001 but no main effect for gender, F(1,300) 5 0.030, P 5 0.86. There were also no interaction effects, indicating that the magnitude of difference in TAS scores between males and females across both groups was equal F(1,300) 5 2.01, P 5 0.16. Indeed, as per the BAQ results, the group classification of with or without ASD was found to be the significant variable influencing mean TAS scores in this present study. Independent-samples Welch’s t-test revealed that there was a statistically significant difference between mean TAS scores for the ASD group (M 5 10.43, SD 5 4.65), and the group without ASD (M 5 14.42, SD 5 3.62), t(103) 5 6.743, Mdiff 5 23.99, 95% CI [22.82, 25.16], P < 0.001, d 5 21.02, Fmax 5 1.66. Specifically, those in the ASD group reported a significant hyporeactivity in thirst/satiety awareness compared to the group without ASD, and this was a large effect. To investigate the relationship between thirst awareness and fluids consumed, a correlational analysis between TAS scores and reported average amount of fluids consumed per day was undertaken. In the group without ASD, a weak positive relationship was found,
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r(226) 5 0.21, P 5 0.002, 95% CI [0.08, 0.33]. Specifically, as TAS scores increased, the average amount of fluids consumed per day also increased. Within the ASD group, however, no relationship was found, r(72) 5 0.09, P 5 0.43, 95% CI [20.14, 0.33].
This study aimed to address the current gap in the literature with regard to how adults with and without ASD interpret elements of the interoceptive sense, and specifically to what extent there may be differences between the two groups in their reported perception of body awareness. If those with ASD have difficulty in perceiving when they are thirsty, hungry, or ill, a better understanding in this regard may help provide improved outcomes for adults with ASD. Strategies could include designing sensory inclusive interventions and self-awareness programmes which may help those with ASD to cope with the stresses of everyday life. The results from the current study provide support for Craig’s characterization of interoception as a distinct sense of the physiological condition of the body. Strong internal consistency across all item responses, for both groups, suggest that perceptions of temperature, thirst, hunger, satiety etc. form together as part of this unique sensory afferent pathway. First, it was anticipated that there would be differences between the two groups in their self-reported BAQ scores, and this was supported. Specifically, those in the ASD group reported a statistically significant hyporeactivity in body awareness compared to the control group, and this was a large effect. The results showed a distinct ASD population, one which consistently reported a low awareness of internal bodily states compared to the control group. Analysis of Variance revealed that mean BAQ scores were not affected by gender in both groups, with females reporting similar body awareness to males. Specifically, males and females in the ASD group reported significantly lower body awareness, compared to controls. This was an unexpected result, as previous research utilizing the BAQ found that females were more likely to report higher body awareness than males in those without ASD [Shields et al., 1989]. Researchers suggested that females may be generally more internally focused and introspective than males, enhancing the ability to detect nonemotive bodily sensations. Subsequent studies utilizing the BAQ, as well as this current study however, have found no difference between males and females in the general perception of body awareness [Baas, Beery, Allen, Wizer, & Wagoner, 2004; Shields & Simon, 1991]. It may be that the original
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results reflected sampling variability rather than a generalized higher body awareness in females. Indeed, other researchers suggest that the interoceptive sense is an “urge for action,” [Jackson, Parkinson, Kim, € ermann, & Eickhoff, 2011], is innate and nonSchu learned, equally present in males and females [McGlone et al., 2012]. It was proposed that there would be differences between the two groups in their self-reported TAS scores, and this was also supported. Specifically, those in the ASD group reported a statistically significant hyporeactivity in thirst/satiety awareness compared to those without ASD, and this was a large effect. Again, this was a distinct ASD population, one which consistently reported a lower awareness of the thirst/satiety response. The TAS was designed as part of this study to measure the construct of nonemotive thirst awareness and satiety, as this is a prominent aspect of the interoceptive sense which is not included in the BAQ. As such, it was important that the refined TAS was able to reliably discern the subtle homeostatic bodily cues that alert to the typical thirst/satiety response, in line with the construct of the BAQ. While the initial factor analysis revealed three components, only the refined three item TAS was deemed to measure this construct. Demographic analysis of the TAS results also revealed that the mean TAS scores were not affected by gender, with females reporting similar thirst awareness/satiety to males. Indeed, the diagnosis of ASD was found to be the overall contributing variable to the differences in mean scores, both for the BAQ and the TAS in this present study. These findings also support the model proposed by Uddin and Menon [2009] where they proposed that those with ASD may have a difficulty in responding to salient interoceptive stimuli, as the AI is pivotal in detecting changes in bodily states. Their model posited that this may be evidenced as a sensory agnosia, or a modality-specific failure of recognition. Previous fMRI studies in adults with ASD have found that one of the areas consistently showing significant hypoactivity is the right AI, compared to controls, and researchers proposed that an appropriate level of AI activity is needed to initiate brain responses to salient stimuli [Di Martino et al., 2009; Menon & Uddin, 2010; Uddin & Menon, 2009]. They suspected that the hypoactivity may be due to a disconnect between the sensory and limbic structures that project to the AI, leading to a reduction in salience detection [Uddin & Menon, 2009]. Whether there is a general sensory agnosia arising from insufficient activation of the AI, however, has not been specifically tested with this study. An alternative framework is that there is a general difficulty for adults with ASD to introspect and focus attention toward the self, and further research is recommended to explore the relationship.
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Also, the results from the current study provided further quantitative support to qualitative studies that found that those with ASD are often unaware of their own body sensations, and for example, do not feel hunger [Bogdashina, 2003; Elwin, et al., 2012]. This study found that interoceptive sensory abnormalities were not reported by adults with ASD as either a hyperreactivity or hyporeactivity (or a combination of both), but a generalized hyporeactivity to internal stimuli. These results are in contrast to previous studies examining external stimuli (sights and sounds etc.), which have found multiple sensory presentations in people with ASD. The results of the current study, at least for the interoceptive sense, however, show a unified low awareness for those on the Autism Spectrum. As there has been very little research on interoception itself, it cannot be assumed that those with ASD process internal information the same way as they process external information. Further research is, therefore, suggested to investigate whether individuals with ASD have different perceptions of internal and external stimuli. It was also anticipated that there would be differences between the two groups in the relationship between self-reported TAS scores and fluid drinking behaviors, and this was partially supported. Correlational analyses between mean TAS scores and average amount of fluids consumed per day revealed that those in the control group showed a significant weak positive relationship between thirst awareness and amount of fluids consumed per day, while those in the ASD group did not show any relationship. Specifically, those in the ASD group were just as likely to consume large amounts of fluid (120 glasses per day) if they reported very low thirst awareness, or very low amounts of fluid (1–3 glasses per day) if they reported higher awareness. Implications and Future Research The results of the current study showed that this is valuable research, and warrants being expanded across domains. Indeed, Keen [2008] noted that disturbances of self-regulatory and homeostatic processes are frequently observed clinically in people with ASD, but as yet has been poorly researched. For example, they suggested that difficulties with hunger and thirst perception would have major implications in the aetiology of some eating disorders, which have been observed in people with ASD [Keen, 2008]. It has been widely reported that children with ASD have unusual eating and drinking behaviors, but the aetiology has been difficult to ascertain. As such, expanding research on interoceptive awareness and functioning is critical to
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extending the understanding of how these physiological processes may be contributing to ASD. A limitation to the current study is that the majority of those in the ASD group reported being diagnosed with Asperger’s Syndrome (n 5 65), which is generally considered to be on the higher functioning end of the Autism Spectrum. Whether the findings can be generalized to the entire ASD population needs to be explored with further research. However, the results of the current study demonstrated that adults with ASD have difficulty with interpreting thirst, hunger, temperature, satiety and the prediction of the onset of illness, compared to a control group. This is an important clinical finding, as difficulties with sensing internal bodily states could theoretically impact on many aspects of a person’s life, including physical and mental health, social interactions, self-awareness, and communication. Based on the findings of this preliminary study, further research is suggested in this regard.
Conclusion This study has found that adults with ASD experience unusual awareness of elements of the interoceptive sense, compared to a control group. While prior research has found that sensory perceptions in people with ASD can either be hyperreactivity or hyporeactivity to external stimuli, or a combination of both, this study has found that adults with ASD reported a unified hyporeactivity to elements of the interoceptive sense, compared to controls. As the DSM-5 includes hyperreactivity or hyporeactivity to sensory input as a subcriterion for diagnosis of ASD, the results of this study are an important clinical finding, both for diagnosis and for the design of interoceptive self-awareness programmes to provide better outcomes for those on the spectrum.
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