Psychiatry Research 245 (2016) 491–496

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Psychiatry Research
journal homepage: www.elsevier.com/locate/psychres

Affective touch awareness in mental health and disease relates

to autistic traits – An explorative neurophysiological investigation
Ilona Croy a,b,n, Helen Geide b, Martin Paulus c, Kerstin Weidner a, Håkan Olausson b
a
Department of Psychotherapy and Psychosomatic Medicine, Technische Universität Dresden, Germany
b
Center for Social and Affective Neuroscience, Department of Clinical and Experimental Medicine, Linköping University, Linköping, Sweden
c
Laureate Institute for Brain Research, Tulsa, OK, USA

art ic l e i nf o a b s t r a c t

Article history: Affective touch is important for social interaction within families and groups and there is evidence that
Received 21 April 2016 unmyelinated C tactile fibers are involved in this process. Individuals with autism spectrum disorders
Received in revised form show alterations in the perception and processing of affective touch. sThus, we hypothesized that af-
29 August 2016
fective touch awareness based on C tactile fiber activation is impaired in individuals with high levels of
Accepted 8 September 2016
autistic trait. The pleasantness perception of optimal and suboptimal C tactile stimuli was tested in an
Available online 13 September 2016
explorative study in 70 patients recruited from an outpatient psychotherapy clinic and 69 healthy
Keywords: comparison subjects. All participants completed questionnaires about autistic traits, depressive symp-
Autism tomatology, childhood maltreatment, and about the daily amount of touch. Relative to comparison
Touch
subjects, patients reported engaging in touch less frequently in daily life and rated touch less pleasant.
Social
Reduced valence ratings of touch were explained by childhood maltreatment but not by any particular
C-tactile
Relationship disorder or depression severity. Among all tested variables, the affective touch awareness correlated with
Childhood maltreatment autistic traits only - in patients as well as in comparison subjects. Taken together, individuals with mental
health issues have a lower baseline of expression and reception of affective touch. Autistic traits and
childhood maltreatment modulate the experience of affective touch.
& 2016 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Taken together, interpersonal touch has a pronounced function in

Interpersonal touch is highly important for human interaction
and “provides the most emotional of our tactile experiences”
(Gallace and Spence, 2010). Touch is sensed from the very first
moments of life, when the newborn is comforted by the mother´s
embrace and remains pivotal during the whole lifespan (Sehlstedt
et al., 2015). Interpersonal touch is not only a powerful way to
convey emotions between individuals (Hertenstein et al., 2006),
but also decreases stress perception (Grewen et al., 2003) and
stress related cortisol response (Ditzen et al., 2007). Moreover,
even subtle interpersonal touch can have strong behavioral con-
sequences: Waiters for instance receive higher tips when touching
their customers (Crusco and Wetzel, 1984), basketball players
perform better the more they touch each other at the beginning of
the season (Kraus et al., 2010), and being touched by a nurse de-
creases levels of stress before surgery (Whitcher and Fisher, 1979).
n
Corresponding author at: Department of Psychotherapy and Psychosomatic
Medicine, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden,
Germany.
E-mail address: Ilona.croy@tu-dresden.de (I. Croy).
social behavior, such as the creation and strengthening of bonds
(for review see (McGlone et al., 2014) and (Gallace and Spence,
2010)).
The ability to process and perceive the whole range of tactile
stimulations may be a precondition for the creation of social bonds
and in consequence for the maintenance of mental health. Indeed,
a positive attitude towards interpersonal touch is negatively cor-
related to social reticence (Fromme et al., 1989) and socially high-
anxious people experience interpersonal touch more aversive than
low anxious ones (Wilhelm et al., 2001). Individuals with autism, a
disorder involving the lack of functional social interaction, are
known to dislike interpersonal touch and 70% of those also exhibit
tactile sensory-perceptual abnormalities (Baranek et al., 2006). An
interesting study on postnatal depression further showed, that
such mothers have problems in creating a rewarding tactile in-
teraction with their baby, which leads to decreased positive re-
sponse in the babies (Malphurs et al., 1996).
Interestingly, research from the last decade opens new possi-
bilities to examine the processing and perception of tactile sti-
mulations. This research shows that there is a group of un-
myelinated afferent nerve fibers, which are specialized in the

http://dx.doi.org/10.1016/j.psychres.2016.09.011
0165-1781/& 2016 Elsevier Ireland Ltd. All rights reserved.
492 I. Croy et al. / Psychiatry Research 245 (2016) 491–496

detection of interpersonal touch. These so called C tactile afferents 2. Methods

are located in the hairy skin of the body and respond to slowly
moving, caressing types of touch (Löken et al., 2009). They re- 2.1. Participants
spond optimally at a stimulus temperature of about 32 °C, i.e. si-
milar to human skin temperature (Ackerley et al., 2014b). The C Seventy patients presenting to outpatient psychotherapy (60
women, 10 men, aged 24–70 years, mean 46.0 712.0 years SD)
tactile fibers do not only have distinct response properties, but
were included in the study. The patients were recruited by four
also project to distinct brain areas, mainly to the posterior insula
psychotherapists and diagnosed by their attending psychothera-
cortex (Björnsdotter et al., 2009). Further, C tactile targeted stimuli
pist according to the international classification of mental and
activate regions known to be involved in reward processing such behavioral disorders, version 10 (Dilling et al., 1991). The sample
as the putamen and the orbitofrontal cortex (Sailer et al., 2016; was unbalanced in gender reflecting the distribution in outpatient
Olausson et al., 2002), and regions implied in processing of social psychotherapy. The majority of patients suffered from mood and
stimuli, such as the social superior temporal sulcus (Bennett et al., affective disorders (ICD 10 F3: n¼ 24 patients), somatoform dis-
2013; Voos et al., 2013). orders (F45: n¼ 18 patients), disorders of personality (F60: n¼22
Microneurography recordings from nerves innervating the patients), post traumatic stress disorder (F43.1: n ¼4 patients), or
human forearm skin show that C tactile fibers respond optimally anxiety disorders (F40/41: n¼ 1 patient) as primary diagnosis.
to stimulation with a velocity of 1–10 cm/s; stimulations per- Most patients (n¼ 45) were diagnosed with more than one mental
formed with a velocity of 0.3 cm/s or slower or with a velocity of disease. Mood and affective disorders (F3: n ¼18 patients), post
30 cm/s or faster are less effective in activating C tactile fibers and traumatic stress disorder (F43.1 n ¼20 patients) and anxiety dis-
especially fast stimulation does not excite those fibers (Ackerley orders (F40/41: n ¼10 patients) were frequently observed co-
morbidities. As we intended to have a broad spectrum of diseases,
et al., 2014b; Löken et al., 2009; Olausson et al., 2010). Accordingly,
no diagnosis was excluded. Patients reported significantly more
light, slow stroking stimulation performed with a velocity of about
adverse childhood experience compared to comparison subjects
1–10 cm/s is perceived more pleasant than stimulation with a fast
(CTQ: emotional abuse: p o0.001; physical abuse: p o0.001, sex-
velocity of 30 cm/s or with a superslow velocity of 0.1 or 0.3 cm/s.
ual abuse: p¼ 0.02; emotional neglect: p o0.001, physical neglect:
With those response characteristics, C tactile fibers are highly po 0.001). Patients and comparison subjects did not differ in
sensitive to human interpersonal stroking touch (Olausson et al., medication, except for antidepressants (43% in patients; 0% in
2010). The velocity dependent pleasantness rating curve has been comparison subjects), analgesics (17% in patients; 4% in compar-
replicated several times - on different body parts (Ackerley et al., ison subjects) and tranquilizer (13% in patients; 0% in comparison
2014a), with handheld as well as robot guided stroking stimula- subjects; compare Table 1).
tion (Triscoli et al., 2013), and for touch in various visual (Ellingsen Physical conditions that are likely to impact touch perception,
et al., 2013) or olfactory conditions (Croy et al., 2014). However, such as diabetes, diseases of liver, kidney, neurological diseases,
there are individual differences, which suggest that several top- history of brain surgery, and any skin diseases on tested side (left
down modulatory processes play a substantial role in the sub- dorsal forearm) were exclusion criteria. Further, all patients were
jective perception of the afferent information carried by C tactile required to be fluent in German, in order to understand the
questionnaires.
fibers. While most people strongly prefer slow over fast stroking,
Sixty-nine healthy participants were recruited by public an-
some are rather indifferent. We hypothesize that any abnormal-
nouncements and among the acquaintances of the examiners (56
ities in C tactile touch perception are likely seen in the domain of
women, 13 men, aged 21–67 years, mean 45.6 712.5 years SD).
social behavior and mental health. The same exclusion criteria as for the patients were applied. Fur-
Although studies on touch in psychiatric disorders are rare, it ther, participants of the control group were required not to be
has been reported that adults with autism are more sensitive than under any psychological treatment and were screened for mental
healthy controls to certain aspects of touch including vibration, health with the short version of the patient health questionnaire
texture perception and thermal pain (Cascio et al., 2008). There are (Löwe and Spitzer, 2001; Spitzer et al., 1999).
a few published examinations on C tactile processing and autism. The study was conducted according to the Declaration of
Those show that the perception and cortical processing of slow
stroking, C tactile targeted stimuli is reduced in adults with high Table 1
Medication in patients and control subjects. The number of participants within a
traits of autism compared to adults with low autistic scores (Voos
group is displayed for each group of drugs.
et al., 2013), and in autistic compared to normally developed
children (Kaiser et al., 2015). In line, recent findings point in the Controls Patients
N N
direction, that autism is related to small fiber loss - affecting C
tactile fibers (Silva and Schalock, 2016). A study in mice further Analgesics 2 13
shows that experimental reduction of peripheral tactile sensitivity Antihypertensives 13 14
Antidiabetics 0 0
leads to enhanced anxiety behavior and reduced social interaction
Lipid lowering drugs 0 0
in mice (Orefice et al., 2016). Thyroid drugs 4 10
Here, we examined if C tactile perception is abnormal in a Ulcus drugs 2 8
broader range of mental disorders and if such abnormality might Arthritis drugs 0 2
Anticoagulants 0 3
provide a functional biomarker of mental disease. In order to Vitamins 2 4
capture the effect of a variety of mental disorders on affective Antidepressiva 0 30
touch perception, an explorative study was set up including pa- Neuroleptica 1 6
Tranquilizer 0 9
tients with various diseases and symptom severity. As adverse Anticonvulsants 0 3
childhood experience is related to mental disorders (Anda et al., Hormonal substances 12 9
2006), childhood experience was further assessed in all Immunosuppressant agents 0 4
Other medication 2 11
participants.
 I. Croy et al. / Psychiatry Research 245 (2016) 491–496
Helsinki and approved by the local ethical board of the University
of Dresden (EK 65022014).
2.2. Experimental setting and procedure
Participants were asked to sit in a comfortable chair in front of
a computer screen with their left arm in prone position on a pillow
positioned on the left side of the chair. The stimuli were applied to
the subject's left dorsal forearm. On the subject's right side, a vi-
sual analog rating scale (VAS) was placed, which was used by the
participants to rate the stimuli.
The stroking was performed in proximo-distal direction by a
trained experimenter (author HG) with a flat, 50 mm wide, soft
brush made of fine, smooth, goat's hair. Prior to the experiment
she was trained in delivering the stimuli with a constant force of
0.4 N using a scale. The experimenter marked an area of 10 cm on
the participants forearm and brush stroking was applied within
this area. During the experiment, the experimenter was visually
guided regarding brushing velocity by a visual meter (on a monitor
not visible to the subject). In total, 15 stroking stimuli were pre-
sented: Stroking with 0.3; 1; 3; 10 and 30 cm/s. Each stroking
velocity was repeated three times and the order of the stimuli was
pseudorandomized. Interstimulus interval was set to 10 s. The
pleasantness ratings obtained from stroking performed by hand
under such controlled conditions are comparable to high-precision
brushing delivered by a robot (Triscoli et al., 2013). After each
stimulus, participants rated the pleasantness on the VAS scale with
the endpoints 0 ¼not pleasant at all to 10 ¼extremely pleasant.
To control for general rating bias in mental disorders, such as
tendency to less pleasant ratings, all participants were asked to
rate how pleasant they perceived five different pictures taken from
the international affective picture system (Lang et al., 1999). Five
pictures of different hedonic quality (spider 1202; smiling baby
2071; clothespins 7052; gold bars 8500; dirty toilet 9301) were
presented for 3 s each on a computer screen with an interstimulus
interval of 10 s. Each picture was presented three times and pre-
sentation order was randomized within and between participants.
After each picture presentation, participants rated the perceived
pleasantness on the VAS presented above.
2.3. Questionnaires
In order to get a broad overview over the patients symptoma-
tology and potential factors that could influence touch perception,
all participants answered the following questionnaires: 1) BDI II
(Beck et al., 1996; Hautzinger et al., 2006) which is a worldwide
used reliable and valid instrument which asks about depression
symptoms with 21 items and was used to measure depression
severity. 2) The Autism spectrum quotient (Woodbury-Smith et al.,
2005) questionnaire which measures high functioning autism with
50 items that relate to social and communication skills, imagina-
tion, attention to details, and tolerance of change. 3) The 28 item
childhood trauma questionnaire CTQ (Bernstein et al., 1997),
which measures childhood maltreatment retrospectively on the
scales emotional and physical neglect and emotional, physical and
sexual abuse. 4) Participants were also asked about their re-
lationship status and with an unstandardized 1-item question
about “how often they experience physical contact to other per-
sons” (410 times/day, 45 times/day, 45 times/week, weekly,
less than weekly).
2.4. Statistical analysis
Data was analyzed with SPSS 21. The pleasantness ratings of
touch were averaged over the three repetitions of each velocity,
and the pleasantness ratings of pictures were averaged over the
493
three repetitions of each picture. The relationship between touch
pleasantness ratings and stroking velocity and differences in
overall or velocity dependent pleasantness ratings were analyzed
with a full factorial repeated measurement ANOVA with the be-
tween subject factor group (2) and the within subject factor ve-
locity (5). For control purposes, the same analysis was repeated
with picture pleasantness ratings. Data is presented after Green-
house-Geisser correction to adjust for violations of the sphericity
assumption.
Several analyses of covariance were conducted: first, to ex-
amine whether medication significantly affected the subjective
perception of C tactile afferent stimulation, the analysis of touch
ratings was repeated with the additional covariate medication (yes
no). This was done for 1) intake of any medication 2) all medica-
tions that differed significantly between groups. Second, the same
analysis was repeated under inclusion of age and gender as cov-
ariate, as age and gender effects in the perception of C tactile sti-
muli have been previously observed (Croy et al., 2014; Sehlstedt
et al., 2016).
Two outcome variables were defined: 1) the overall touch
pleasantness calculated as the mean of all touch pleasantness
ratings and 2) the affective touch awareness calculated as
the difference of pleasantness ratings between C tactile opti-
mized and non-optimized stroking (3 vs 30 cm/s, compare
(Ackerley et al., 2014b; Löken et al., 2009; Olausson et al.,
2010)), weighted by the overall pleasantness ratings (affe-
ctive touch awareness ¼ Xpleasantness3 cm/s  Xpleasantness30 cm/s)*
(∑(Xpleasantness0.3 cm/s , Xpleasantness1 cm/s, Xpleasantness3 cm/s,
Xpleasantness10 cm/s, Xpleasantness30 cm/s)/5). Over the whole sam-
ple, there was a weak correlation between both scores (r ¼ 0.2,
p ¼ 0.01). Normal distribution of those variables was checked
with the Kolmogorov-Smirnov test, and patients and compar-
ison subjects were compared using independent sample t-test.
Six regression analyses were performed with automatic linear
modeling: two for the whole sample, two for patients, and two
for comparison subjects with the target variable A) overall
touch pleasantness and B) affective touch awareness. The pre-
dictors age, sex, depression score, autism spectrum quotient
score, amount of interpersonal touch, and childhood maltreat-
ment were included. For childhood maltreatment, the mean of
the whole questionnaire was used. Focusing on patients, the
same model was computed and extended by a predictor of the
diagnoses observed more than 10 times (F3; F43; F40/41; F45;
F60). Group differences between the reported frequencies of
interpersonal touch were analyzed with the non-parametric
Mann-Whitney test. The reported frequencies of interpersonal
touch were correlated to the overall touch pleasantness and to
affective touch awareness using Spearman correlation in pa-
tients and comparison subjects, separately.
3. Results
3.1. Patients liked touch less, but there were no group differences in
affective touch awareness or in hedonic perception of control pictures
There was a significant main effect of velocity (F[137,4] ¼72.9,
po 0.001, ŋ2 ¼0.35), with velocities in the intermediate range
being rated as more pleasant compared to fast or very slow ve-
locities (Fig. 1), and there was a significant quadratic fit of the
pleasantness curve (F[138,1]¼ 191.6, p o0.001, ŋ2 ¼0.58). Ratings
differed significantly between groups (F[138,1] ¼5.9, p ¼0.018,
ŋ2 ¼ 0.04), with patients rating touch less pleasant compared to
controls. However, there was no significant interaction between
velocity and group (F[138,1]¼1.7, p ¼0.18). Thus, patients differed
from comparison subjects in overall touch pleasantness (T[138] ¼
494 I. Croy et al. / Psychiatry Research 245 (2016) 491–496
2.4, p¼ 0.017, d ¼0.36), but not in affective touch awareness(T
[138] ¼0.8, p¼ 0.4). Inclusion of medication as covariate in the
model did not change the effects and there was no significant
main or interaction effect of medication. Inclusion of age and
gender did not change the effects and there was no significant
main or interaction effect of age or gender.
The overall touch pleasantness and affective touch awareness
were fairly normally distributed in both groups. Five of the com-
parison subjects (7.2%) scored o/¼ 0 in affective touch awareness,
indicating that they did not prefer C tactile targeted over non C
tactile targeted touch. Nine of the patients (12.9%) scored o /¼0.
In contrast to the touch ratings, there was no significant main effect
of group (F[138,1]¼ 0.15, p¼ 0.7) and no significant group*stimulus
interaction (F[138,1]¼0.1, p¼1) for the picture ratings.
3.2. Overall touch perception related to diagnosis, affective touch
Fig. 1. Affective touch perception in psychotherapeutic outpatients (N ¼ 70) and
healthy comparison subjects (N¼ 69). A) Patients and comparison subjects pre-
ferred intermediate, C tactile targeted, stroking velocities (po 0.001). Patients rated
all velocities as less pleasant than comparison subjects (p¼ 0.018). There were no
significant differences in the shape of the curve between patients and comparison
subjects.
Fig. 2. Affective touch awareness in healthy comparison subjects (N ¼69) and in patients (N¼ 70). Affective touch awareness represents the perceived pleasantness dif-
ference between C tactile optimized and suboptimized stimuli. High scores indicate a preference for C tactile optimized stroking stimuli, and low scores indicate a preference
for C tactile suboptimal stimuli. Affective touch awareness was negatively related to autistic traits, both in comparison subjects (r¼  0.27, p ¼ 0.025) and in patients
(r¼  0.33, p ¼ 0.006).
awareness to autistic traits
The overall touch pleasantness was not very well related to any
of the predictors. In the whole sample, a diagnose of personality
disorder was related to reduction of overall touch pleasantness, (F
[151,1] ¼13.3, p o0.001) explaining 7.5% of variance in total. Spe-
cifically for the patients group, overall touch pleasantness was
related to personality disorders as well (F[69,1] ¼5.3, p ¼0.025,
10.8% explained variance). For comparison subjects on the other
hand, sex had a weak relation in tendency, with women rating
touch more pleasant than men. However this result did not reach
significance level (F[68,1]¼ 3.6, p ¼0.06, 3.8% explained variance),
and the result has to be interpreted with caution due to the un-
balanced gender distribution.
Affective touch awareness on the other hand was related to the
autism spectrum quotient, both, in patients and in comparison
subjects. Across all participants, a model that included the autism
spectrum quotient (F[149,1] ¼7.3, p ¼0.007) and the history of
childhood maltreatment (CTQ: (F[149,1]¼4.2, p ¼0.042) explained
9.2% of the variance. Low scores in the autism spectrum quotient
and high scores in history of childhood maltreatment were related
to enhanced affective touch awareness. In the patients, the model
explained 12.3% of the variance and was mainly influenced by the
autism spectrum quotient (F[69,1]¼ 7.4, p ¼0.008). For comparison
subjects, the model explained 6.0% in total and only autism
spectrum quotient (F[69,1] ¼5.3, p ¼0.025), but none of the other
variables, contributed. Hence, autism spectrum quotient was cor-
related to affective touch perception in patients (r¼  0.33,
p¼ 0.006; Fig. 2) as well as in comparison subjects (r ¼  0.27,
p¼ 0.025; Fig. 2). Further, a diagnose of personality disorder con-
tributed to the model, but did not reach significance (F[149,1]¼ 3.7,
p¼ 0.057), and likewise a diagnose of post traumatic stress dis-
order contributed, but did not reach significance (F[69,1] ¼3.1,
p¼ 0.083).
An exploratory analysis was conducted to examine whether
there was a similar relationship in the opposite direction: did af-
fective touch awareness also relate to the autism spectrum quo-
tient? Therefore, autism spectrum quotient was used as target and
affective touch awareness as well as all the previous variables
served as predictors. For patients, the model with best fit (27.3%
explained variance) included depression scores (F[69,1]¼ 14.1,
po 0.001), affective touch awareness (F[69,1] ¼6.0, p ¼0.017) and
sex (F[69,1] ¼4.3, p ¼0.041). For comparison subjects the model
with best fit (15.0% explained variance) included the same vari-
ables as for the patients; depression scores (F[68,1]¼6.6,
 I. Croy et al. / Psychiatry Research 245 (2016) 491–496
Fig. 3. Frequency of interpersonal touch in healthy comparison subjects (N ¼69) and patients (N¼ 70). Overall, patients report significantly (p o 0.001) less interpersonal
touch compared to comparison subjects (compare the two large pie diagrams). This pattern was independent of whether participants were single, in a relation or in a
relationship with shared household (compare the six small plots).
p ¼0.013), affective touch awareness (F[68,1] ¼5.0, p¼ 0.028), and
sex (F[68,1] ¼3.1, p ¼0.081).
3.3. Patients reported less interpersonal touch
Most of the healthy comparison subjects reported to be tou-
ched more than 10 times a day, and none of them reported in-
terpersonal touch less than 5 times a week. Most of the patients
however, reported to be touched more than 5 times a day and
there were patients reporting to be touched less than weekly
(Fig. 3). Overall, patients reported significantly less interpersonal
touch as compared to controls (Z¼4.9, p o0.001, compare Fig. 3).
Regardless of whether patients lived alone, were in a relationship
or were in a relationship with a shared household, and regardless
of whether patients lived together with children or not, they re-
ported less interpersonal contact compared to healthy controls
(Fig. 3). Overall, there were no significant correlations between the
reported amount of interpersonal touch and overall touch plea-
santness or affective touch awareness.
4. Discussion
Both patients and healthy comparison subjects showed the
expected velocity dependent pleasantness curve for brush strok-
ing, indicating that C tactile targeted stroking velocities were
preferred over slower and faster velocities (Löken et al., 2009).
However, patients rated touch generally less pleasant than com-
parison subjects. This effect was especially pronounced in patients
with disorders of personality. The attenuation of overall plea-
santness of touch might be due to specific reductions of hedonic
tone of tactile stimulation or rely on other influencing factors such
as being less comfortable in interpersonal interactions in general.
However, one needs to be careful to directly relate the hedonic
tone of C tactile stimulation to the preference of touch in daily life.
It is not clear whether the subjective preference of a variety of
different interpersonal touch situations directly relate to hedonic
evaluation of C tactile stimulation. This needs to be evaluated in
future studies.
In line with the reduced appraisal of touch, patients reported a
generally reduced amount of interpersonal touch frequency. This
was true regardless of whether patients were single, in a re-
lationship, or in a relationship with shared household. Inter-
personal touch reflects emotional bonds between people and
those who are emotionally close also allow others to touch them
more frequently (Suvilehto et al., 2015). However, the reason for a
reduction in frequency of reported touch is unclear. Among the
495
possibilities are that patients avoid interpersonal touch, live in
relationships that are characterized by reduced body contact, or
exhibit memory bias. Nevertheless, given that interpersonal touch
presumably strengthens social bonds, a reduced amount seems
not beneficial for patients with mental disorders.
The experimental condition was designed to enable valid
comparisons between ratings of C tactile optimal and sub-optimal
stimuli as reflected by the affective awareness score. Our patients
and comparison subjects showed the typical velocity dependent
pleasantness rating curve (compare for instance (Ackerley et al.,
2014a, 2014b; Ellingsen et al., 2013; Löken et al., 2009; Olausson
et al., 2010; Triscoli et al., 2013). However, consistent with pre-
vious observations, there were some people in both groups who
had a negative affective touch awareness score, indicating that
they rated non-C tactile targeted stroking as more pleasant than C
tactile targeted stroking. The affective touch awareness was sig-
nificantly and specifically related to the autism spectrum quotient.
However, sample characteristics, ascertainment approach, and the
lack of other covariates limits the degree to which these results
might generalize. Nevertheless, our finding is consistent with
previous studies showing that healthy adult people with autistic
traits (measured with the same autism spectrum questionnaire as
in the current study) as well as children with diagnosed autism
spectrum disorder have a reduced appraisal of C tactile targeted
stroking stimuli (Kaiser et al., 2015; Voos et al., 2013).
In contrast to these studies (Kaiser et al., 2015; Voos et al., 2013),
we did not limit our sample to a specific diagnosis but examined a
representative sample of outpatient psychotherapeutic patients. In-
terestingly, we found for both patients and healthy comparison
subjects that autistic traits and not depression severity or other de-
mographic characteristics (sex and age) related to the affective touch
awareness. These findings suggest that quantifying the degree of
affective touch awareness might be a potential trans-diagnostic
biomarker for autistic traits. In addition, adverse childhood experi-
ence was also related to affective touch awareness in both groups.
However, this effect was weaker and, surprisingly, negatively corre-
lated to affective touch awareness, i.e. the more adverse childhood
experiences the higher the affective touch awareness.
Social impairment is one of the key domains of the autism
spectrum quotient and it has been suggested, that C tactile per-
ception is important for social communication and bonding (Löken
and Olausson, 2010; McGlone et al., 2014). This notion is not only
underpinned by the typically social situation of touch but also by
neural pathways. C tactile fibers project to target areas of posterior
insula, OFC (Olausson et al., 2002) and also activate superior
temporal cortex (Bennett et al., 2013; Voos et al., 2013). The su-
perior temporal sulcus is considered a “social brain area” (Pelphrey
496 I. Croy et al. / Psychiatry Research 245 (2016) 491–496
et al., 2004), and it is possible that there is a shift of touch pro-
cessing from affective to discriminative networks in people with
prominent autistic traits (Kaiser et al., 2015). However, a labeled
line view of affective and discriminative touch very much sim-
plifies neuronal mechanisms of perception and spinal dorsal horn
signal integration is likely to contribute but is yet poorly under-
stood (Abraira and Ginty, 2013). However, recent research in-
dicates that impairments of peripheral tactile nerve fiber proces-
sing are related to social behavior in mice (Orefice et al., 2016).
Peripheral C tactile signaling and affective touch perception are
remarkably well correlated; the frequency of nerve firing corre-
lates at r4 0.9 with pleasantness ratings (Löken et al., 2009). Im-
paired affective touch awareness is observed in people with re-
duced C fiber density (Morrison et al., 2011). Moreover, the pre-
ference of fast or slow stroking is a rather stable trait with a retest
reliability of 0.77 (Croy et al., 2015). Further studies are needed
that examine the specificity and sensitivity of affective touch
awareness in patients with autism spectrum disorders.
In perspective, such studies may promote the utility of affective
touch awareness as a diagnostic marker for autism and reveal
clinical usability. Already now, therapeutic applications of slow
stroking touch for enhancement of social processing in autism
spectrum diseases (Silva et al., 2015) are in line with our ob-
servations. Another interesting perspective is the research on ef-
ferent C fiber function. Studying both branches of the post-
ganglionic C-fiber system will clarify, whether affective touch re-
lates to autonomic dysfunction and cardiovascular risk in patients
with psychiatric disorders.
In summary, the findings from the current study point toward
affective touch awareness as a biological marker that is closely
related to autistic traits rather than as a vulnerability marker for
mental disorders in general.
Acknowledgements
This study was supported by a grant of the Marcus och Amalia
Wallenbergs Minnesfond to IC (MAW 2014.000).
References
Abraira, V.E., Ginty, D.D., 2013. The sensory neurons of touch. Neuron 79 (4),
618–639.
Ackerley, R., Carlsson, I., Wester, H., Olausson, H., Wasling, H.B., 2014a. Touch per-
ceptions across skin sites: differences between sensitivity, direction dis-
crimination and pleasantness. Front. Behav. Neurosci. 8.
Ackerley, R., Wasling, H.B., Liljencrantz, J., Olausson, H., Johnson, R.D., Wessberg, J.,
2014b. Human C-tactile afferents are tuned to the temperature of a skin-
stroking caress. J. Neurosci. 34 (8), 2879–2883.
Anda, R.F., Felitti, V.J., Bremner, J.D., Walker, J.D., Whitfield, C., Perry, B.D., Dube, S.R.,
Giles, W.H., 2006. The enduring effects of abuse and related adverse experi-
ences in childhood. Eur. Arch. Psychiatry Clin. Neurosci. 256 (3), 174–186.
Baranek, G.T., David, F.J., Poe, M.D., Stone, W.L., Watson, L.R., 2006. Sensory ex-
periences questionnaire: discriminating sensory features in young children
with autism, developmental delays, and typical development. J. Child Psychol.
Psychiatry 47 (6), 591–601.
Beck, A.T., Steer, R.A., Brown, G.K., 1996. Beck Depression Inventory-II. San Antonio.
Bennett, R.H., Bolling, D.Z., Anderson, L.C., Pelphrey, K.A., Kaiser, M.D., 2013. fNIRS
detects temporal lobe response to affective touch. Soc. Cogn. Affect. Neurosci. 9
(4), 470–476.
Bernstein, D.P., Ahluvalia, T., Pogge, D., Handelsman, L., 1997. Validity of the
childhood trauma questionnaire in an adolescent psychiatric population. J. Am.
Acad. Child Adolesc. Psychiatry 36 (3), 340–348.
Björnsdotter, M., Löken, L., Olausson, H., Vallbo, Å., Wessberg, J., 2009. Somatotopic
organization of gentle touch processing in the posterior insular cortex. J.
Neurosci. 29 (29), 9314–9320.
Cascio, C., McGlone, F., Folger, S., Tannan, V., Baranek, G., Pelphrey, K.A., Essick, G.,
2008. Tactile perception in adults with autism: a multidimensional psycho-
physical study. J. Autism Dev. Disord. 38 (1), 127–137.
Croy, I., Angelo, S.D., Olausson, H., 2014. Reduced pleasant touch appraisal in the
presence of a disgusting odor. PLoS One 9 (3), e92975.
Croy, I., Triscoli, C., Luong, A., Sehlstedt, T., Sailer, U., Olausson, H., 2015. The In-
dividual Preferred Velocity of Touch as a Stable Measurement. IASAT, London.
Crusco, A.H., Wetzel, C.G., 1984. The midas touch the effects of interpersonal touch
on restaurant tipping. Personal. Soc. Psychol. Bull. 10 (4), 512–517.
Dilling, H., Mombour, W., Schmidt, M.H., 1991. Internationale Klassifikation psy-
chischer Stö rungen: ICD-10, Kapitel V (F, klinisch-diagnostische Leitlinien).
Ditzen, B., Neumann, I.D., Bodenmann, G., von Dawans, B., Turner, R.A., Ehlert, U.,
Heinrichs, M., 2007. Effects of different kinds of couple interaction on cortisol
and heart rate responses to stress in women. Psychoneuroendocrinology 32 (5),
565–574.
Ellingsen, D.-M., Wessberg, J., Eikemo, M., Liljencrantz, J., Endestad, T., Olausson, H.,
Leknes, S., 2013. Placebo improves pleasure and pain through opposite mod-
ulation of sensory processing. Proc. Natl. Acad. Sci. 110 (44), 17993–17998.
Fromme, D.K., Jaynes, W.E., Taylor, D.K., Hanold, E.G., Daniell, J., Rountree, J.R.,
Fromme, M.L., 1989. Nonverbal behavior and attitudes toward touch. J. Non-
verbal Behav. 13 (1), 3–14.
Gallace, A., Spence, C., 2010. The science of interpersonal touch: an overview.
Neurosci. Biobehav. Rev. 34 (2), 246–259.
Grewen, K.M., Anderson, B.J., Girdler, S.S., Light, K.C., 2003. Warm partner contact is
related to lower cardiovascular reactivity. Behav. Med. 29 (3), 123–130.
Hautzinger, M., Keller, F., Kühner, C., 2006. Beck Depressions-inventar (BDI-II).
Harcourt Test Services Frankfurt.
Hertenstein, M.J., Keltner, D., App, B., Bulleit, B.A., Jaskolka, A.R., 2006. Touch
communicates distinct emotions. Emotion 6 (3), 528.
Kaiser, M.D., Yang, D.Y., Voos, A.C., Bennett, R.H., Gordon, I., Pretzsch, C., Beam, D.,
Keifer, C., Eilbott, J., McGlone, F., Pelphrey, K.A., 2015. Brain mechanisms for
processing affective (and nonaffective) touch are atypical in autism. Cereb.
Cortex.
Kraus, M.W., Huang, C., Keltner, D., 2010. Tactile communication, cooperation, and
performance: an ethological study of the NBA. Emotion 10 (5), 745.
Lang, P.J., Bradley, M.M., Cuthbert, B.N., 1999. International Affective Picture System
(Iaps): Instruction Manual And Affective Ratings. The Center for Research in
Psychophysiology, University of Florida.
Löken, L.S., Olausson, H., 2010. The skin as a social organ. Exp. Brain Res. 204 (3),
305–314.
Löken, L.S., Wessberg, J., McGlone, F., Olausson, H., 2009. Coding of pleasant touch
by unmyelinated afferents in humans. Nat. Neurosci. 12 (5), 547–548.
Löwe, B.P., Spitze, R.L., 2001. Gesundheitsfragebogen für Patienten PHQ-D: Manual
(Komplettversion und Kurzform). Pfizer GmbH.
Malphurs, J.E., Field, T.M., Larraine, C., Pickens, J., Pelaez-Nogueras, M., Yando, R.,
Bendell, D., 1996. Altering withdrawn and intrusive interaction behaviors of
depressed mothers. Infant Ment. Health J. 17 (2), 152–160.
McGlone, F., Wessberg, J., Olausson, H., 2014. Discriminative and affective touch:
sensing and feeling. Neuron 82 (4), 737–755.
Morrison, I., Loken, L.S., Minde, J., Wessberg, J., Perini, I., Nennesmo, I., Olausson, H.,
2011. Reduced C-afferent fibre density affects perceived pleasantness and
empathy for touch. Brain: J. Neurol. 134 (Pt 4), 1116–1126.
Olausson, H., Lamarre, Y., Backlund, H., Morin, C., Wallin, B., Starck, G., Ekholm, S.,
Strigo, I., Worsley, K., Vallbo, Å., 2002. Unmyelinated tactile afferents signal
touch and project to insular cortex. Nat. Neurosci. 5 (9), 900–904.
Olausson, H., Wessberg, J., Morrison, I., McGlone, F., Vallbo, A., 2010. The neuro-
physiology of unmyelinated tactile afferents. Neurosci. Biobehav. Rev. 34 (2),
185–191.
Orefice, L.L., Zimmerman, A.L., Chirila, A.M., Sleboda, S.J., Head, J.P., Ginty, D.D.,
2016. Peripheral mechanosensory neuron dysfunction underlies tactile and
behavioral deficits in mouse models of ASDs. Cell.
Pelphrey, K.A., Morris, J.P., Mccarthy, G., 2004. Grasping the intentions of others:
the perceived intentionality of an action influences activity in the superior
temporal sulcus during social perception. J. Cogn. Neurosci. 16 (10), 1706–1716.
Sailer, U., Triscoli, C., Häggblad, G., Hamilton, P., Olausson, H., Croy, I., 2016. Tem-
poral dynamics of brain activation during 40 min of pleasant touch.
NeuroImage.
Sehlstedt, I., Ignell, H., Backlund Wasling, H., Ackerley, R., Olausson, H., Croy, I.,
2016. Gentle touch perception across the lifespan. Psychol. Aging 31 (2), 176.
Sehlstedt, I., Ignell, H., Wasling, H.B., Ackerley, R., Olausson, H., Croy, I., 2015. Gentle
touch perception across the lifespan. Psychol. Aging.
Silva, L., Schalock, M., 2016. First skin biopsy reports in children with autism show
loss of C-tactile fibers. J. Neurol. Disord. 4 (262), 2.
Silva, L.M., Schalock, M., Gabrielsen, K.R., Budden, S.S., Buenrostro, M., Horton, G.,
2015. Early intervention with a parent-delivered massage protocol directed at
tactile abnormalities decreases severity of autism and improves child-to-parent
interactions: a replication study. Autism Res. Treat., 2015.
Spitzer, R.L., Kroenke, K., Williams, J.B., Patient Health Questionnaire Primary Care
Study Group, 1999. Validation and utility of a self-report version of PRIME-MD:
the PHQ primary care study. JAMA 282 (18), 1737–1744.
Suvilehto, J.T., Glerean, E., Dunbar, R.I., Hari, R., Nummenmaa, L., 2015. Topography
of social touching depends on emotional bonds between humans. Proc. Natl.
Acad. Sci., 19231.
Triscoli, C., Olausson, H., Sailer, U., Ignell, H., Croy, I., 2013. CT-optimized skin
stroking delivered by hand or robot is comparable. Front. Behav. Neurosci. 7,
208.
Voos, A.C., Pelphrey, K.A., Kaiser, M.D., 2013a. Autistic traits are associated with
diminished neural response to affective touch. Soc. Cogn. Affect. Neurosci. 8 (4),
378–386.
Whitcher, S.J., Fisher, J.D., 1979. Multidimensional reaction to therapeutic touch in a
hospital setting. J. Personal. Soc. Psychol. 37 (1), 87.
Wilhelm, F.H., Kochar, A.S., Roth, W.T., Gross, J.J., 2001. Social anxiety and response
to touch: incongruence between self-evaluative and physiological reactions.
Biol. Psychol. 58 (3), 181–202.
Woodbury-Smith, M.R., Robinson, J., Wheelwright, S., Baron-Cohen, S., 2005.
Screening adults for asperger syndrome using the AQ: a preliminary study of its
diagnostic validity in clinical practice. J. Autism Dev. Disord. 35 (3), 331–335.