Content uploaded by Marcel Kinsbourne
Author content
All content in this area was uploaded by Marcel Kinsbourne on Apr 24, 2014
Content may be subject to copyright.
http://aut.sagepub.com/
Autism
http://aut.sagepub.com/content/10/2/155
The online version of this article can be found at:
DOI: 10.1177/1362361306062021
2006 10: 155Autism
Miriam Liss, Celine Saulnier, Deborah Fein and Marcel Kinsbourne
Sensory and attention abnormalities in autistic spectrum disorders
Published by:
http://www.sagepublications.com
On behalf of:
The National Autistic Society
can be found at:AutismAdditional services and information for
http://aut.sagepub.com/cgi/alertsEmail Alerts:
http://aut.sagepub.com/subscriptionsSubscriptions:
http://www.sagepub.com/journalsReprints.navReprints:
http://www.sagepub.com/journalsPermissions.navPermissions:
http://aut.sagepub.com/content/10/2/155.refs.htmlCitations:
What is This?
- Apr 13, 2006Version of Record >>
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
155
Sensory and attention
abnormalities in autistic
spectrum disorders
MIRIAM LISS University of Washington, Fredericksburg, USA
CELINE SAULNIER Yale Child Study Center, New Haven,USA
DEBORAH FEIN University of Connecticut,Storrs, USA
MARCEL KINSBOURNE New School University, New
York, USA
ABSTRACT Individuals with autistic spectrum disorders (ASDs)
often experience, describe and exhibit unusual patterns of sensation
and attention. These anomalies have been hypothesized to result from
overarousal and consequent overfocused attention. Parents of indi-
viduals with ASD rated items in three domains, ‘sensory overreactiv-
ity’, ‘sensory underreactivity’ and ‘sensory seeking behaviors’, of an
expanded version of the Sensory Profile, a 103-item rating scale
developed for the present study. Parents also rated symptom severity,
overselective attention and exceptional memory, and completed the
Vineland Adaptive Behavior Scales. Of 222 rated subjects, 144 had
complete data. Cluster analysis showed the predicted overfocused
pattern of sensation and attention, comprising overreactivity, persever-
ative behavior and interests, overfocused attention and exceptional
memory in 43 percent of this sample. This pattern was striking in 10
percent. The neurological basis of overreactivity and overfocusing is
discussed in relation to the overarousal hypothesis. Attention is drawn
to its considerable prevalence in the ASD population.
ADDRESS Correspondence should be addressed to: MIRIAM LISS, Department of
Psychology, University of Mary Washington, 1301 College Avenue, Fredericksburg, VA
22401, USA. e-mail: mliss@umw.edu
Introduction
Individuals with autistic spectrum disorders (ASDs) often respond in
unusual ways to sensory stimuli (see Freeman et al., 1984). Some also
describe themselves as being oversensitive to certain stimuli to the point
of being impelled to withdraw from them (Grandin, 1996). Yet, conversely,
individuals with ASD often underreact to stimuli, for instance ignoring
autism © 2006
SAGE Publications
and The National
Autistic Society
Vol 10(2) 155–172; 062021
1362-3613(200603)10:2
www.sagepublications.com
DOI: 10.1177/1362361306062021
KEYWORDS
attention;
autism;
autistic
spectrum
disorder;
cluster
analysis;
sensory
behavior
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
painful bumps or bruises (Ornitz, 1988). Although such deviant reactions
to sensory stimuli have been repeatedly remarked upon, they are not
featured in the extensive symptom list for autistic disorder offered in DSM-
IV (American Psychiatric Association, 1994). Also, individuals with autism
engage in repetitive behaviors that have been thought to induce sensory
self-stimulation. We have termed the three patterns of behavior listed above
‘overreactivity’, ‘underreactivity’ and ‘seeking’ respectively. They may char-
acterize subgroups of individuals with ASD, or alternative states of indi-
viduals with ASD.
Impairment in sensory modulation and directing attention featured so
prominently among the questionnaire responses of parents of 242 indi-
viduals with autism that Ornitz (1988) nominated this difficulty as the
cause of autism. On Dunn’s (1999) Sensory Profile, an instrument sensi-
tive to anomalous sensorimotor behavior, 32 individuals with autism
scored significantly higher than controls on 85 percent of the items, across
all factors. Watling et al. (2001) found that eight of 10 Sensory Profile
factor scores of 40 children with autism indicated abnormality relative to
matched controls. According to Dunn et al. (2002), a group of 42 children
with Asperger syndrome scored abnormally relative to controls on 22 of
23 Sensory Profile items. By what means might these pervasive sensory and
attentional anomalies arise?
We hypothesize that sensory overreactivity may be explained as a
possible response to overarousal. Specifically, overarousal might lead to
overselective attention with secondary overreactivity.
Many individuals with autism exhibit overselective attention, typically
focusing on a single element in a complex array (Lovaas and Schreibman,
1971; Lovaas et al., 1979). Shifting this focus may be difficult, leading to
perseverative behavior. Overarousal leads to a narrowing of the range of
cue utilization, rendering attention overselective (Easterbrook, 1959).
Waterhouse et al. (1996) in turn related sensory disturbances to exagger-
ated selective attention. Exaggerated focus on elementary features of objects
might amplify the children’s experience of sounds, sights, and touches,
triggering overreactivity. They also attributed perseverative preoccupations
and repetitive movements, classified as seeking behavior, to overselective
attention, as when the child is preoccupied with elementary surface
features of objects (the spinning of a top, or hands waved in front of the
face). Since individuals with autism may concentrate on small details of the
environment for an inordinate amount of time, filtering out peripheral
stimuli, they may develop savant skills and high-fidelity memory with
respect to these details. Kinsbourne (1980) remarked on similarities
between repetitive movements, here termed ‘sensory seeking’, and
‘displacement’ behavior that is observed in animals when they are in
AUTISM 10(2)
156
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
overaroused states of frustration or thwarting. Displacement behaviors
appear to serve to moderate arousal levels.
We propose that a subset of individuals with autism will exhibit a
pattern of sensory overreactivity in combination with an exaggerated or
overfocused selective attention. Thus, we hypothesize that individuals with
sensory overreactivity will also exhibit characteristics such as (1) other
manifestations of overfocused behavior, such as not being able to shift
attentional focus, (2) perseverative preoccupation, and resulting from the
latter, (3) exceptional memory for self-selected material.
If such a cluster emerges, its prevalence in the sample population will
be of interest. Is it sufficiently prominent to deserve mention in diagnos-
tic symptom lists?
Methods
Procedure
Surveys and return envelopes were distributed at local and national confer-
ences for parents of children with ASD and through the mail via an ASD
network newsletter. Parents were told about the survey, and were asked to
complete it and to return it either in person or through the mail. They were
told that results of the survey would remain anonymous. Participating
parents signed an informed consent form to have their data analyzed, and
for an hour-long follow-up telephone interview. Parents were not paid for
their participation, but were provided with a summary of research results
when the investigation was concluded.
Participants
Inclusion criteria were (1) previous diagnosis on the ASD spectrum by a
psychologist, psychiatrist or neurologist and (2) current diagnosis on the
ASD spectrum based on answers given on a DSM-IV checklist included in
the package of an initial group of 252. Twenty-nine participants were
dropped from the analysis because they did not meet both criteria, and one
was dropped on account of exceptionally high scores on the Vineland
(e.g. socialization SS = 134). The final sample consisted of 222 parent
reports. One hundred and ninety-one parents participated in the follow-
up interview and were also administered the Vineland Adaptive Behavior
Scales (Sparrow et al., 1984) by telephone. Complete data sets were avail-
able on 144 children.
Demographic information and mean scores on all experimental vari-
ables are presented in Table 1.
LISS ET AL.: SENSORY AND ATTENTION ABNORMALITIES
157
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
Materials
Parents were given a packet that included the following materials.
Sensory Questionnaire This 103-item questionnaire, designed for this
investigation (Liss et al., 1998; Saulnier et al., 2002), utilized 60 items
from the Sensory Profile (Dunn, 1999) with permission from the author
and publisher. These were supplemented with 43 newly developed items
that reflected specific sensory behaviors seen in individuals with autism.
Items are rated on a 1–5 Likert scale. Higher scores indicate greater impair-
ment. Factor analysis of the standardization sample of 181 children and
adolescents with ASD revealed a first factor, termed stimulus seeking, a
second factor, termed overreactivity, and a third factor, termed underreac-
tivity. These factors accounted for 34, 14 and 10 percent of the variance
respectively, 58 percent accounted for collectively (Saulnier et al., 2002).
Ninety-five items clearly fell on one of the three factors (the 43 items we
developed, and 52 items from the Sensory Profile). The additional eight
items were related to endurance, tone, body position and movement, and
did not fall clearly on any of the factors; these items were not used in
further analyses. The additional 43 items used, the 52 item numbers from
the Sensory Profile, and our coding system, which indicated which items
were taken to indicate overreactivity, underreactivity and seeking, respec-
tively, can be seen in Appendix 1.
Parents also rated the extent to which their child had an exceptional
memory, on a 1–5 Likert scale.
AUTISM 10(2)
158
Table 1 Mean scores on experimental variables (N = 144)
Variable (possible range) Mean (SD)
% male 79.9
Age in months 102.4 (50.1)
Exceptional memory (1–5) 4.1 (1.2)
Overreactivity (1–5) 2.36 (0.54)
Underreactivity (1–5) 2.36 (0.66)
Sensory seeking (1–5) 2.01 (0.53)
DSM-IV social symptoms (1–7) 4.12 (1.8)
DSM-IV communication impairment (1–7) 4.70 (1.4)
DSM-IV perseveration (1–7) 3.57 (1.2)
Kinsbourne Overfocusing Scale (0–75) 44.4 (13.6)
Vineland communication standard score 66.2 (24.6)
Vineland daily living standard score 53.0 (19.4)
Vineland socialization standard score 60.4 (14.2)
Vineland adaptive behavior composite standard score 56.4 (16.7)
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
DSM-IV checklist The wording was kept consistent with the DSM,
although for many items (such as impaired gestures, or perseveration on
parts of objects) examples were provided to clarify the item. Parents rated
their children on a 1–7 Likert scale: (1) symptom is not present, (3) mild
impairment, (5) moderate impairment and (7) severe impairment. Mean
scores were calculated for social symptoms, communication impairment,
and perseveration.
Kinsbourne Overfocusing Scale Kinsbourne (1991) designed this 25-
item checklist (see Appendix 2) to assess behaviors of some children
referred for attention deficit hyperactivity disorder (ADHD), but whose
attention seemed to be overfocused rather than lacking focus (Kinsbourne
and Caplan, 1979). Parents rated their children on whether they exhibited
the listed behaviors over the past 6 months: (0) never, (1) sometimes, (2)
pretty often, and (3) very often. The range of possible scores was 0–75.
Factor analysis revealed a first factor, which can be described in terms of
perseveration and social withdrawal, in a normative as well as a clinical
sample. On the Personality Inventory for Children, the clinical sample was
identified with 90 percent accuracy as distinct from mainstream ADHD, in
terms of the factors of withdrawal and social incompetence (Kinsbourne,
unpublished data).
Vineland Adaptive Behavior Scale At follow-up, the Vineland Adaptive
Behavior Scales (Sparrow et al., 1984) were administered over the phone.
The Vineland evaluates how well a child functions in his or her day-to-day
environment. Standard scores and age equivalents are provided in the
communication, socialization, and daily living domains. Standard scores
for these domains, as well as the adaptive behavior composite, were used
in the analyses.
Results
Data screening
All variables met the assumptions of normality as a precondition for para-
metric statistics, except exceptional memory, which was highly negatively
skewed. A reverse log transformation resulted in an acceptably normal
distribution. Lower scores on this transformed variable correspond to
higher exceptional memory abilities.
LISS ET AL.: SENSORY AND ATTENTION ABNORMALITIES
159
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
Correlations with experimental measures
Table 2 presents correlations between the experimental measures and the
Sensory Questionnaire subscales (overreactivity, underreactivity and
sensory seeking).
Overreactivity was significantly positively correlated with age; older
individuals tend to have higher overreactivity scores. Overreactivity was
also significantly positively correlated with social symptoms and persever-
ation impairments on the DSM-IV checklist, as well as lower socialization
scores on the Vineland. It was highly correlated with the Kinsbourne Over-
focusing Scale total score. Overreactivity was unrelated to communication
impairment on the DSM-IV checklist or to communication abilities on the
Vineland Adaptive Behavior Scales. Overreactivity was negatively correlated
with the reverse log of the exceptional memory scale; being overreactive
to stimuli is related to having a greater exceptional memory.
Underreactivity was strongly positively related to all dimensions of
autistic symptomatology, as well as daily living scores on the Vineland and
the adaptive behavior composite (the higher the underreactivity scores, the
lower the adaptive functioning scores). It was positively correlated with the
Kinsbourne Overfocusing Scale ratings, although less so than overreactiv-
ity. There was no relationship between underreactivity and age, or excep-
tional memory.
Sensory seeking behavior decreased with increasing age. Like under-
reactivity, it was related to greater symptom severity in all domains. It was
also related to lower daily living and communication scores on the Vineland
as well as the adaptive behavior composite. It was also positively correlated
with overfocusing scores, although not as strongly as overfocusing was
correlated with overreactivity.
AUTISM 10(2)
160
Table 2 Correlations between Sensory Survey and other variables (N = 144)
Overreactivity Underreactivity Sensory seeking
Age 0.171* n.s. –0.220**
DSM-IV social symptoms 0.269** 0.463** 0.164*
DSM-IV communication impairment n.s. 0.224** 0.316**
DSM-IV perseveration 0.268** 0.282** 0.332**
Kinsbourne Overfocusing Scale 0.608** 0.293** 0.235**
Vineland communication n.s. n.s. –0.263**
Vineland daily living n.s. –0.326** –0.165*
Vineland socialization –0.195* n.s. n.s.
Vineland adaptive behavior composite n.s. –0.221** –0.235**
log R exceptional memory –0.196* n.s. n.s.
* p < 0.05; ** p < 0.01.
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
Subscale intercorrelations
The three subscales of the Sensory Survey were significantly intercorrelated.
The bivariate correlation between overreactivity and underreactivity was
r = 0.343 (p < 0.001). The bivariate correlation of sensory seeking to
overreactivity was r = 0.460 and to underreactivity was r = 0.545 (both
p < 0.001).
Cluster analysis
A hierarchical agglomerative cluster analysis was performed in order to test
the theoretical prediction that overreactivity, perseverative behavior, over-
focusing, and high-fidelity memory would cluster together in the same
individuals. Severity of symptomatology measured by the DSM-IV inter-
view (range 0–7), communication, socialization and daily living standard
scores on the Vineland Adaptive Behavior Scales, Kinsbourne Overfocusing
Scale total score, Sensory Questionnaire overreactivity, underreactivity and
sensory seeking mean scores, DSM-IV interview social symptoms,
communication impairment and perseveration scores, and the transformed
exceptional memory variable were entered into the analysis. All other vari-
ables met the assumptions of normality and linearity.
Clustering was determined by Ward’s (1963) method, the procedure
that is most frequently used for considering all possible combinations of
clusters. Squared Euclidean distance was used as the similarity measure.
Variables were standardized to control for unequal scaling that can affect
cluster results. To determine the number of clusters, both the hierarchical
tree and the agglomeration schedule were examined. Four clusters
appeared to differentiate groups of subjects adequately. These four clusters
were then subjected to a K-means iterative partitioning clustering
procedure (Punj and Stewart, 1983). This method lets any misassigned
subjects be relocated to a more appropriate cluster and allows for the lowest
within-cluster variance and the highest between-cluster variance. Further
supporting the four-cluster solution, only 16 of 144 subjects (11 percent)
were reassigned to different clusters after the iterative partitioning. Thus,
the clusters were relatively stable.
The final cluster centers that used standardized scores for the four
groups can be seen in Table 3. One-way ANOVAs using Tukey post hoc tests
were conducted on the unstandardized variables to examine group differ-
ences. Means and standard deviations as well as group differences at the
0.05 level for each cluster on the unstandardized scores can be seen in Table
4. Although the results are identical for the transformed exceptional
memory item, the original item is used for ease of interpretation.
Cluster 1 included 17 individuals. It featured overreactivity to sensory
stimuli, perseverative behavior on the DSM-IV, high overfocusing scores on
LISS ET AL.: SENSORY AND ATTENTION ABNORMALITIES
161
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
the Kinsbourne Overfocusing Scale, and an exceptional memory for selec-
tive material. Thus, this group has high scores on all the variables that are
highlighted by the theory of overfocused selective attention.
Cluster 2 characterized 36 individuals. It had the lowest scores on the
Sensory Survey and was least impaired on the DSM-IV interview. It also
AUTISM 10(2)
162
Table 4 Characteristics of four clusters (N = 144)
1234
Overfocused No sensory Low Mildly
problems functioning overfocused
n = 17 n = 36 n = 44 n = 47
Mean (SD) Mean (SD) Mean (SD) Mean (SD)
Vineland communication SS 90.7 (20.3)
a
73.0 (20.7)
a
49.7 (18.2)
b
76.6 (22.3)
a
Vineland daily living SS 68.5 (17.1)
a
62.0 (12.9)
ac
38.5 (17.8)
b
54.2 (17.2)
c
Vineland socialization SS 60.8 (11.5)
ab
69.4 (11.2)
b
52.0 (12.6)
a
61.2 (14.3)
a
Kinsbourne Overfocusing Scale
total 61.2 (9.5)
a
30.2 (10.7)
b
45.0 (10.9)
c
48.7 (7.9)
c
Overreactivity 3.0 (0.61)
a
1.9 (0.35)
b
2.4 (0.42)
c
2.5 (0.41)
c
Underreactivity 2.5 (0.59)
ac
1.8 (0.42)
b
2.9 (0.59)
c
2.2 (0.52)
a
Sensory seeking 2.4 (0.52)
a
1.7 (0.39)
b
2.3 (0.48)
a
1.8 (0.40)
b
DSM social symptoms 5.2 (1.1)
a
3.2 (0.70)
b
4.8 (0.97)
a
3.9 (0.98)
c
DSM communication impairment 5.3 (1.3)
a
4.4 (1.3)
b
5.6 (1.2)
a
3.9 (1.1)
c
DSM perseveration 4.9 (1.2)
a
2.7 (0.96)
b
4.0 (1.1)
c
3.3 (0.90)
d
Does your child have an exceptional
memory? 4.9 (0.49)
a
3.8 (1.4)
b
3.3 (1.3)
b
4.8 (0.46)
a
Age in months: mean (SD) 114.2 (46.4)
ab
80.7 (37.2)
a
97.5 (50.0)
a
119.2 (54.1)
b
% male 88 83 70 83
a–d
Numbers with different superscripts are significantly different at p < 0.05 by Tukey post hoc.
Table 3 Final cluster centers
Cluster
1234
Z-score: communication SS 0.98 0.27 –0.65 0.42
Z-score: daily living standard score 0.84 0.51 –0.69 0.11
Z-score: socialization standard score 0.08 0.65 –0.50 0.11
Z-score: Kinsbourne Overfocusing Scale 1.40 –0.89 0.21 0.47
Z-score: overreactivity mean score 1.25 –0.85 0.06 0.19
Z-score: underreactivity mean score 0.30 –0.84 0.83 –0.13
Z-score: seeking mean score 0.74 –0.63 0.54 –0.45
Z-score: DSM social symptoms 0.78 –0.86 0.51 –0.35
Z-score: DSM communication impairment 0.31 –0.33 0.52 –0.68
Z-score: DSM perseveration 1.03 –0.72 0.32 –0.26
Z-score: log R exceptional memory –0.72 0.26 0.65 –0.58
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
included the lowest overfocusing scores. Individuals in cluster 2 are rela-
tively high functioning, are not seriously impaired, and have few sensory
problems.
Cluster 3 consisted of 44 individuals. It had the lowest adaptive func-
tioning scores, and high underreactivity and sensory seeking scores. This
group is characterized by communication impairments and social
symptoms. Their degree of perseveration is second only to that of cluster
1. Overall, this cluster is low functioning, with prominent undersensitiv-
ity and sensory seeking.
Cluster 4 had 47 individuals. Their scores were relatively low on autistic
symptomatology, and relatively high on adaptive functioning, sensory over-
reactivity (although not as high as cluster 1), overfocusing, and having an
exceptional memory. When a three-cluster solution is forced, this cluster
combines with cluster 1. However, including this cluster with cluster 1
obscures the unique overfocusing qualities of cluster 1. Cluster 4 can be
considered mildly overfocused.
Group differences on demographic variables can be seen in Table 4.
There is a significant group difference for age F(3, 140) = 4.8, p < 0.01.
Post hoc analyses indicated that cluster 4 was significantly older than clusters
2 and 3. Cluster 3 had relatively more girls than the other clusters, but this
difference failed to reach significance.
Group differences on experimental variables can be seen in Table 4. The
significance of the F-statistic for the variables used in the cluster analysis is
not useful, as clusters were grouped to create the biggest differences
between clusters on these variables. However, post hoc testing indicates
which of the groups differ from each other. Cluster 1 had significantly
higher scores than all other clusters on overreactivity, overfocusing, and
DSM-IV perseveration. It had equal impairment in social symptoms and
communication impairment on the DSM-IV to cluster 3, the low-function-
ing cluster. Cluster 2 had lower overreactivity and underreactivity, as well
as DSM-IV social symptom and perseveration scores, than all other groups.
Clusters 1 and 4 had significantly higher exceptional memory scores than
the other two clusters.
Individual DSM-IV items were examined by cluster. Clusters 1 and 3
had the most impaired scores for most of the social symptom items, and
were not significantly different from each other. Clusters 2 and 4 had less
impaired scores and were not significantly different from each other. The
item ‘prefers to be alone’ was significantly more endorsed in cluster 1 than
in any other group, and was significantly less endorsed in cluster 2 than in
all other groups. In the communication impairment domain, cluster 3
featured the most ‘delay of expressive and receptive language’, and cluster
1 the least. Cluster 3 was least able to initiate and sustain a conversation,
LISS ET AL.: SENSORY AND ATTENTION ABNORMALITIES
163
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
but cluster 1 used the most idiosyncratic and stereotyped language
(although not significantly more than cluster 3). In social and imitative
play skills, clusters 1 and 3 were the most impaired, and not different from
each other. Cluster 1 has the most impaired scores for all diagnostic criteria
in the perseverative category, and cluster 3 has the second most impaired
scores. Cluster 1 was significantly more notable for preoccupation with
parts of objects, and preoccupation with specific interests, than all other
groups.
Discussion
We delineated the nature and extent of sensory disturbances in ASD, and
tested the hypothesis that sensory overreactivity is related to overselective
or overfocused attention. We hypothesized that a subset of individuals
would exhibit both overreactive and overfocused attention. These indi-
viduals may disproportionately assign attention to a central focus, thus
amplifying the subjective experience of sensory stimuli.
Our hypothesis was confirmed by the results of the cluster analysis.
Some 10 percent of the sample had scores indicative of an overreactive,
overselective, and overfocused attentional system. They had high scores on
overreactivity, exhibited overfocused behaviors (as rated on the Kinsbourne
Overfocusing Scale), exhibited perseverative and stereotyped behavior (as
measured by the DSM-IV checklist), and had a high-fidelity memory. They
were relatively high functioning, and had the highest mean communi-
cation scores on the Vineland of the four clusters. Their sensory seeking
scores were relatively high, although not significantly higher than those of
the low-functioning cluster. A milder form of the same behavioral pattern
was seen in a larger group of children.
Although the overfocusing cluster was the highest functioning, it was
the most socially impaired. Overfocusing, therefore, appears detrimental to
social behavior, but not necessarily detrimental to intellect and behavior in
general. Overarousal may specifically impede social interaction (Dawson
and Lewy, 1989). Conversely, cluster 3, the lowest-functioning cluster,
tended to be underreactive. Underreactivity may be related to mental retar-
dation.
Sensory seeking behaviors were highly prevalent in the overfocused
cluster. An overreaction may only occur when an unexpected or otherwise
aversive stimulus reaches the attentional focus. But an individual with
autism may actively choose a pleasurable stimulus to focus on, finding it
fascinating and perhaps soothing (Gillingham, 2000) and an escape from
more disturbing input. Repeating the choice would be seen as sensory
seeking behavior.
AUTISM 10(2)
164
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
Overfocused attention may be mistaken for the inattention of ADHD,
and Kinsbourne (1991) developed the Kinsbourne Overfocusing Scale to
differentiate this relatively small subgroup from the mainstream of ADHD
individuals. He suggested that the overfocused subgroup represents ‘a
dimension of personality that extends the continuum of autistic behavior
into normality’ (1991, p. 32). Although overfocused behavior may be an
isolated pattern in an otherwise normally functioning individual, it appears
from the present findings that it may also characterize a large subgroup of
individuals who have other symptoms of ASD, and in whom the diagnosis
of ASD is not in doubt.
Individuals with autism have been thought to have an unstable arousal
system, and consequently often to be in a state of overarousal (Dawson and
Lewy, 1989; Hutt et al., 1964; Kinsbourne, 1980; 1987). Thus Kinsbourne
attributed autistic symptomatology to fluctuatingly exaggerated ascending
activation of the cortex from the brainstem. Individuals with ASD have
particular difficulty in negotiating social situations, and this may be due to
overarousal because a social context is changeable, unpredictable and often
emotionally arousing. However, an extensive literature does not reach
consensus on whether individuals with ASD are overaroused in a general
sense, at least as judged from EEG and autonomic measures. It seems more
likely that some individual neurotransmitter pathways are overreactive. The
alternative construct of ‘noisy’ firing of cortical neurons has also been
offered (e.g. Hussman, 2001).
Overfocused attention may be related to abnormal neurotransmitter
activity. Kinsbourne (1991) linked overfocusing to dopamine overreactiv-
ity. Correspondingly, amphetamine augments behaviors that are already
common in an animal’s repertoire (Robbins, 1975). Furthermore,
dopamine agonists induce perseveration in mice (Anisman and Kokkini-
dis, 1975) and social withdrawal in rats (Gambill and Kornetsky, 1976).
Stereotyped activities have been linked to excessive dopamine activity in
the nigrostriatal circuitry (Creese and Iversen, 1974). Excessive dopamine
activity in the mesolimbic pathway has been implicated in interpersonal-
perceptual deficits and in the nigrostriatal pathway in motor stereotypies
(Coleman and Gillberg, 1985; Damasio and Maurer, 1978; Maurer and
Damasio, 1982). Dopamine antagonists such as neuroleptics and atypical
antipsychotics have ameliorated symptoms of ASD, including stereotypies
and inattention/hyperactivity, whereas dopamine agonists exacerbated
these symptoms (Anderson et al., 1989; McDougle et al., 1998; Mikkelsen,
1982). Thus, excessive dopamine activity in nigrostriatal and/or mesolim-
bic pathways may play a role in the overreactivity of children with ASD.
Deficient dorsolateral prefrontal control may disinhibit nigrostriatal activity
(Bannon and Roth, 1983), thereby contributing to the psychopathology.
LISS ET AL.: SENSORY AND ATTENTION ABNORMALITIES
165
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
The overarousal hypothesis has been reformulated in terms of ‘noisy’
firing of cortical neurons. Hussman (2001) has implicated disinhibition
due to release of gabaergic inhibition in ASD, which would result in
hyperexcitation of target neurons and therefore difficulty in distinguish-
ing a stimulus from competing ‘noise’. Overreactivity would reflect this
overexcitement of sensory systems. Overfocus and perseveration would be
compensatory behaviors, serving to reduce sensory input into a narrow,
controllable scope. Also implicating increased cortical ‘noise’, Casanova et
al. (2002) reported that microcellular columns in the brains of nine indi-
viduals with autism who were studied at postmortem were smaller, more
numerous and more dispersed in their cellular formation than those of
four matched controls. They suggest that this pattern would lead to over-
connected and insufficiently inhibited neural networks, with consequent
hyperarousal and impaired selection (see also Belmonte and Yurgelun-
Todd, 2003).
Difficulty in shifting attention may contribute to overfocusing and
exacerbate the difficulties associated with overarousal. If individuals with
ASD find it difficult to avert their attention from an aversive stimulus, they
might overreact to it. Switching attention involves dorsolateral prefrontal
cortex, as evidenced by neuropsychological (Godefroy and Rousseaux,
1996) and functional imaging (Barrett et al., 2003) studies. Difficulty
executing rapid shifts of attention may also result from cerebellar dysfunc-
tion, and may undermine social development (Courchesne et al., 1994a).
The slowing of orienting to visual cues was correlated with the degree of
cerebellar hypoplasia in individuals with autism (Harris et al., 1999). Cere-
bellar abnormalities have been found in postmortem and MRI studies of
autism (Courchesne et al., 1994b).
Our findings are consistent with the overarousal hypothesis in any of
the above forms. This hypothesis proposes that individuals with ASD suffer
from overarousal and that this primary difficulty may lead to overselective
attention and repetitive behavior. Overselective attention and repetitive
behavior compensate for the hypothesized hyperaroused state by allowing
the individual with ASD both to focus on, and to generate, predictable
repetitive events to help moderate their arousal level. Our investigation was
not designed to determine causality. However, the fact that overreactivity,
overfocusing, and sensory seeking behaviors clustered together in a
subgroup supports this theoretical position.
Although we did not specifically hypothesize that overeactivity and
overfocusing would be related to sensory underreactivity, there was a
positive correlation between underreactivity and both of these scales. Thus,
it is of theoretical interest to determine whether underreactivity can also
be explained by overarousal or an overfocused attention. Underreactivity
AUTISM 10(2)
166
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
to sensory stimuli may be caused by the same underlying mechanisms as
overreactivity. It may be a matter of the distribution of the individual’s
attention. If a stimulus is directed outside the focus of attention, and does
not elicit orienting or other reaction, then an individual would seem to be
underreactive to that stimulus. Alternatively or additionally, underreactiv-
ity is the aftermath of overarousal so severe that it precipitates a state of
shutdown (Gillingham, 2000), perhaps at the conclusion of a prolonged
bout of dearousing repetitive movements (Kinsbourne, 1980).
As predicted, sensory overreactivity clustered with overfocused and
perseverative behavior, as well as exceptional memory for material of
interest, in subjects who were found to be generally high functioning with
disproportionately impaired social skills. In contrast, sensory underreactiv-
ity was concentrated in a generally low-functioning subgroup. From an
arousal perspective, the high-functioning subgroup would be regarded as
generally overaroused, and their underreactivity might suggest that the
low-functioning group is in general underaroused. However, being under-
reactive does not entail being underactive. The repetitive movement
patterns here characterized as sensory seeking were common in both
subgroups, but more prominent in the low-functioning subgroup. Self-
generated and self-referential movements seem to replace this group’s
reaction to environmental change.
We have suggested that sensory seeking is compensatory, moderating
arousal when it rises to uncomfortable heights. However, repetitive move-
ments were prominent also in underreactive low-functioning participants
with ASD. Indeed, repetitive movements are frequently observed in intel-
lectually impaired individuals who do not have autism (Alvarez, 1999),
in typical children who are in residential care (Troster, 1994), in typical
infants confined in cribs, and in caged or isolated animals (Berkson and
Mason, 1964). They might be situational, in reaction to an environment
that offers few response opportunities to individuals who therefore
become overaroused, but whose response capabilities are limited.
Baumann remarked that ‘[stereotypies] seem to stabilize the child’s level
of arousal in monotonous, frustrating or overstimulating situations’
(1999, p. 602). They are perhaps better described as self-soothing than
stimulation seeking.
The overreactive/overfocused pattern of behavioral abnormality to
some degree characterized nearly half of our study sample, and is there-
fore a major component of autistic spectrum disorders. Diagnostic criteria
typically emphasize deficits and disabilities rather than deviances in
behavior. Nonetheless, the overreactivity/overfocusing symptom pattern
may merit more than its current low level of prominence among the formal
diagnostic criteria for ASD.
LISS ET AL.: SENSORY AND ATTENTION ABNORMALITIES
167
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
Appendix 1: Sensory Questionnaire
The following are the numbers of the 52 items from the Sensory Profile (copyright
© 1999 by the Psychological Corporation, all rights reserved). Also shown is the
domain in which they were included: O = overreactivity, U = underreactivity, S =
stimulus seeking.
1 (O), 2 (O), 4 (O), 5 (O), 6 (U), 7 (U), 8 (S), 9 (O), 10 (O), 15 (O), 18 (O),
19 (O), 20 (O), 21 (O), 25 (S), 26 (S), 27 (S), 28 (S), 29 (O), 30 (O), 32 (O),
33 (O), 35 (O), 36 (O), 38 (O), 39 (O), 40 (S), 41 (S), 42 (U), 43 (U), 44 (S),
45 (S), 46 (U), 50 (U), 53 (S), 54 (O), 55 (O), 56 (O), 57 (O), 58 (O), 59 (S),
60 (S), 64 (S), 65 (S), 77 (O), 78 (O), 81 (S), 83 (S), 87 (O), 89 (O), 96 (O),
99 (U)
The following are the 43 additional items (© by Miriam Liss, Celine A. Saulnier, and
Deborah Fein, 1998; University of Connecticut), again with the domains shown:
O Responds negatively to noisy environments (e.g. shopping malls, crowded restau-
rant).
U Appears not to notice loud and sudden noises (e.g. dishes crashing, sirens).
S Actively seeks loud environments (e.g. prefers noisy cafeteria to quiet classroom).
S Holds hand over ears while vocalizing (e.g. humming, singing).
O Has an adverse reaction to printed words in motion (e.g. credits after a movie).
O Seems to have exceptional peripheral vision (responds to visual cue without
looking directly at it).
O Has a negative reaction (covers eyes) to visually complex environments (e.g.
colorful classroom).
U Does not react to bright lights when shining in their faces.
U Appears not to see things.
S Waves fingers in front of eyes.
S Touches or presses eyeballs.
S Presses face to television.
S Has fixation on moving words (e.g. movie credits).
S Stares at spinning objects for long periods of time.
O Dislikes spinning.
U No reaction to being moved suddenly (being turned upside down, being swung
around in a circle).
U Does not appear to get dizzy when spinning.
S Seeks out swinging.
S Jumps excessively (on bed, floor, etc.).
O Hates cold weather or cold water.
O Has a negative reaction to tags on clothing.
O Has an adverse reaction to light/gentle touch (e.g. tickles).
O Has an adverse reaction to deep pressure (hugs, someone grabbing arm).
U Unresponsive to extreme heat.
U Unresponsive to extreme cold.
U Doesn’t seem to notice light touch.
U Doesn’t seem to notice deep pressure.
U Unresponsive to aversive textures (e.g. sand or rocks in shoes).
S Hits body.
S Bangs head.
AUTISM 10(2)
168
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
S Throws body.
S Bites self.
S Sucks on fingers.
S Picks skin.
S Pulls own hair out.
S Flaps hands.
S Other similar behaviors (list: ___________________________).
O Gags or vomits in response to non-preferred food items.
U Appears unresponsive to strong or spicy foods.
S Shows preference for strong or spicy foods.
O Overreactive to strong odors.
O Can detect/is aversive to faint odors (e.g. body lotion, faint perfume).
S Seeks out certain smells (list: ____________________).
Appendix 2: Kinsbourne Overfocusing Scale
Please rate the child’s behavior on each item listed below over the last 6 months. Please
circle only one of the following ratings:
0 = behavior occurs not at all; 1 = it occurs sometimes; 2 = it occurs pretty often;
3 = it occurs very often
1 Prefers sameness, upset by sudden changes in routine.
2 Socially withdrawn and unskilled, especially with strangers.
3 Works slowly and may be compulsive.
4 Resists being hurried or told to do more than one thing at a time.
5 Organization is difficult (for instance, organizing schoolwork, keeping up with
assignments, cleaning up room), especially at the beginning of tasks.
6 Often seems preoccupied with his/her own thoughts.
7 Is bothered by loud noises.
8 Unusually sensitive hearing.
9 Has a narrow scope of interest.
10 Prefers to focus on one thing at a time.
11 Explores topics of own choosing in depth.
12 Resists shifting attention or changing activities on someone else’s timetable.
13 Worrier, anxious.
14 Overly sensitive to negative feedback.
15 May interpret a parent’s frown as indicating anger or a teacher’s scolding directed
specifically at him/her.
16 Has trouble ‘remembering’ (for instance, remembering more than one instruc-
tion at a time, classroom assignments, chores).
17 Is quietly oppositional, stubborn.
18 May have explosive outbursts, and takes a considerable time to cool off.
19 Performs better on tasks and in situations after getting used to them (for instance,
at the end of the school year than at the beginning, or after trying a task one or
more times).
20 May keep the same posture of facial expression for unusually long periods of time.
21 Is frightened of anticipated new or intense experiences (for instance, meeting new
people or undertaking new activities).
22 Becomes preoccupied with impending, anticipated events.
LISS ET AL.: SENSORY AND ATTENTION ABNORMALITIES
169
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
23 Engages in repetitive movements (for instance, tapping, self-touching).
24 Often sits ‘hunched over’ when working.
25 Is shy.
References
ALVAREZ, N. (1999) ‘Motor Disorders in Persons with Mental Retardation or
Developmental Disabilities’, in
A .B. JOSEPH & R . R . YOUNG (eds) Movement Disorders
in Neurology and Neuropsychiatry, 2nd edn, pp. 623–36. Oxford: Blackwell.
AMERICAN PSYCHIATRIC ASSOCIATION (1994) Diagnostic and Statistical Manual of Mental
Disorders, 4th edn (DSM-IV). Washington, DC: APA.
ANDERSON, G .M ., CAMPBELL, M ., ADAMS, P., SMALL, A .M ., PERRY, R .& SHELL,
J. (1989) ‘The Effects of Haloperidol on Discrimination Learning and Behavioral
Symptoms in Autistic Children’, Journal of Autism and Developmental Disorders 19: 227–39.
ANISMAN, H .& KOKKINIDIS, L . (1975) ‘Effects of Scopolamine, d-Amphetamine
and Other Drugs Affecting Catecholamines on Spontaneous Alternation and
Locomotor Activity in Mice’, Psychopharmacologia 45: 55–63.
BANNON, M .J .& ROTH, R .H . (1983) ‘Pharmacology of Mesocortical Dopamine
Neurons’, Pharmacological Review 35: 53–68.
BARRETT, N.A ., LANGE, M .M ., SMITH, G.L., KARAYANIDIS, F., MICHIE, P.T.,
KAVANAGH, D.J., ET AL. (2003) ‘Human Brain Regions Required Further
Dividing and Switching of Attention between Two Features of a Single Object’,
Brain Research: Cognitive Brain Research 17: 1–13.
BAUMANN, M . (1999) ‘Motor Dysfunction in Autism’, in H .B .J. JOSEPH &
R . R . YOUNG (eds) Movement Disorders in Neurology and Neuropsychiatry, 2nd edn,
pp. 601–5. Oxford: Blackwell.
BELMONTE, M . K .& YURGELUN-TODD, D.A . (2003) ‘Functional Anatomy of
Impaired Selective Attention and Compensatory Processing in Autism’, Cognitive
Brain Research 17: 651–64.
BERKSON, G .& MASON, W.A . (1964) ‘Motor Dysfunction in Autism’, Perceptual and
Motor Skills 19: 635–52.
CASANOVA, M .F., BUXHOEVEDEN, D.P., SWITALA, A .E .& ROY, E . (2002)
‘Minicolumnar Pathology in Autism’, Neurology 58: 428–32.
COLEMAN, M .& GILLBERG, C . (1985) The Biology of the Autistic Syndromes. New York:
Praeger.
COURCHESNE, E ., TOWNSEND, J., AKSHOOMOFF, N. A ., SAITOH, O.,
YEUNG-COURCHESNE, R ., LINCOLN, A .J., ET AL. (1994a) ‘Impairment in
Shifting Attention in Autistic and Cerebellar Patients’, Behavioral Neuroscience 108:
848–65.
COURCHESNE, E ., TOWNSEND, J.& SAITOH, O. (1994b) ‘The Brain in Infantile
Autism: Posterior Fossa Structures Are Abnormal’, Neurology 44: 214–23.
CREESE, I .& IVERSEN, S .D. (1974) ‘The Role of Forebrain Dopamine Systems in
Amphetamine Induced Stereotyped Behavior in the Rat’, Psychopharmacologia 36:
345–57.
DAMASIO, A . R .& MAURER, R .G. (1978) ‘A Neurological Model for Childhood
Autism’, Archives of Neurology 35 (12): 777–86.
DAWSON, G.& LEWY, A . (1989) ‘Reciprocal Subcortical–Cortical Influences in
Autism’, in
G. DAWSON (ed.), Autism: Nature, Diagnosis and Treatment, pp. 144–73. New
York: Guilford.
AUTISM 10(2)
170
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
DUNN, W. (1999) Sensory Profile, User’s Manual. Antonia, TX: The Psychological
Corporation.
DUNN, W., MYLES, B .& ORR, S . (2002) ‘Sensory Processing Issues Associated with
Asperger Syndrome: A Preliminary Investigation’, American Journal of Occupational
Therapy 56: 97–102.
EASTERBROOK, J. A . (1959) ‘The Effect of Emotion on Cue Utilization and the
Organization of Behaviour’, Psychological Review 66: 183–201.
FREEMAN, B .J., RITRO, E . R .& SCHROTH, P.C . (1984) ‘Behavior Assessment of the
Syndrome of Autism: Behavior Observation System’, Journal of the American Academy of
Child Psychiatry 23: 588–94.
GAMBILL, J. D.& KORNETSKY, C . (1976) ‘Effects of Chronic d-Amphetamine on
Social Behavior of the Rat: Implication for an Animal Model of Paranoid
Schizophrenia’, Psychopharmacologia 50: 215–23.
GILLINGHAM, G. (2000) Autism: A New Understanding. Edmonton, Canada: Tacit.
GODEFROY, O.& ROUSSEAUX, M . (1996) ‘Divided and Focused Attention in Patients
with Lesion of the Prefrontal Cortex’, Brain and Cognition 30: 155–74.
GRANDIN, T. (1996) Thinking in Pictures. New York: Vintage.
HARRIS, N., COURCHESNE, E ., TOWNSEND, J ., CARPER, R .& LORD, C. (1999)
‘Neuroanatomic Contributions to Slowed Orienting of Attention in Children with
Autism’, Brain Research: Cognitive Brain Research 8: 61–71.
HUSSMAN, J .P. (2001) ‘Suppressed GABAergic Inhibition as a Common Factor in
Suspected Etiologies of Autism’, Journal of Autism and Developmental Disorders 31: 247–8.
HUTT, C ., HUTT, S . J., LEE, D.& OUNSTED, C. (1964) ‘Arousal and Childhood
Autism’, Nature 204: 908–9.
KINSBOURNE, M . (1980) ‘Do Repetitive Movement Patterns in Children and Animals
Serve a Dearousing Function?’, Developmental and Behavioral Pediatrics 1: 39–42.
KINSBOURNE, M . (1987) ‘Cerebral-Brainstem Relations in Infantile Autism’, in
E . SCHOPLER & G. MESIBOV (eds), Neurobiological Issues in Autism, pp. 107–25. New
York: Plenum.
KINSBOURNE, M . (1991) ‘Overfocusing: An Apparent Subtype of Attention Deficit
Hyperactivity Disorder’, in
N. AMIR, I . RAPIN & D. BRANSKI (eds) Pediatric
Neurology: Behavior and Cognition of the Child with Brain Dysfunction, vol. 1, pp. 18–35. Basel:
Karger.
KINSBOURNE, M .& CAPLAN, P.J. (1979) ‘The Overfocused Child’, in Children’s
Learning and Attention Problems, Chapter 8. Boston, MA: Little, Brown.
LISS, M ., SAULNIER, C .A .& FEIN, D. (1998) The Sensory Survey. University of
Connecticut.
LOVAAS, I .& SCHREIBMAN, L . (1971) ‘Stimulus Overselectivity of Autistic Children
in a Two Stimulus Situation’, Behavior Research and Therapy 9: 305–10.
LOVAAS, I ., KOEGEL, R .& SCHREIBMAN, L . (1979) ‘Stimulus Overselectivity in
Autism: A Review of Research’, Psychological Bulletin 86: 1236–54.
MAURER, R . G.& DAMASIO, A .R . (1982) ‘Childhood Autism from the Point of
Behavioral Neurology’, Journal of Autism and Developmental Disorders 12: 195–205.
MCDOUGLE, C., HOLMES, J., CARLSON, D., PELTON, G., COHEN, D.& PRICE,
L . (1998) ‘A Double-Blind, Placebo-Controlled Study of Risperidone in Adults
with Autistic Disorder and Other Pervasive Developmental Disorders’, Archives of
General Psychiatry 55: 633–41.
MIKKELSEN, E . (1982) ‘Efficacy of Neuroleptic Medication in Pervasive
Developmental Disorders of Childhood’, Schizophrenia Bulletin 8: 320–8.
LISS ET AL.: SENSORY AND ATTENTION ABNORMALITIES
171
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
ORNITZ, E . (1988) ‘Autism: A Disorder of Directed Attention’, Brain Dysfunction 1:
309–22.
PUNJ, G.& STEWART, D. (1983) ‘Cluster Analysis in Marketing Research: Review
and Suggestions for Application’, Journal of Marketing Research 20: 134–48.
ROBBINS, T. W. (1975) ‘The Potentiation of Conditioned Reinforcement by
Psychomotor Stimulant Drugs: A Test of Hill’s Hypothesis’, Paychopharmacologia 45:
103–14.
SAULNIER, C., LISS, M .& FEIN, D. (2002) ‘The Nature of Sensory Abnormalities in
Autism vs. Typical Children’, paper presented at the 2nd Annual International
Meeting for Autism Research, Orlando, FL, November 2002.
SPARROW, S ., BALLA, D.& CICCHETTI, D. (1984) Vineland Adaptive Behavior Scales.
Circle Pines, MN: American Guidance Service.
TROSTER, H . (1994) ‘Prevalence and Functions of Stereotyped Behaviors in
Nonhandicapped Children in Residential Care’, Journal of Abnormal Child Psychology 22:
79–97.
WARD, J .H . (1963) ‘Hierarchical Grouping to Optimize an Objective Function’,
Journal of the American Statistical Association 58: 236–44.
WATERHOUSE, L ., FEIN D.& MODAHL, C. (1996) ‘Neurofunctional Mechanisms in
Autism’, Psychological Review 103: 457–89.
WATLING, R .L ., DEITZ, J.& WHITE, O. (2001) ‘Comparison of Sensory Profile
Scores of Young Children with and without Autism Spectrum Disorders’, American
Journal of Occupational Therapy 55: 416–23.
AUTISM 10(2)
172
at Bobst Library, New York University on November 23, 2012aut.sagepub.comDownloaded from
