Download as pdf or txt
Download as pdf or txt
You are on page 1of 14

VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Psychophysical Assessment of Timing in Individuals


With Autism
Melissa J. Allman and Iser G. DeLeon
Johns Hopkins University School of Medicine and Kennedy Krieger Institute
John H. Wearden
Keele University, Staffordshire, United Kingdom

Abstract
Perception of time, in the seconds to minutes range, is not well characterized in autism. The
required interval timing system (ITS) develops at the same stages during infancy as
communication, social reciprocity, and other cognitive and behavioral functions. The
authors used two versions of a temporal bisection procedure to study the perception of
duration in individuals with autism and observed quantifiable differences and characteristic
patterns in participants’ timing functions. Measures of timing performance correlated with
certain autism diagnostic and intelligence scores, and parents described individuals with
autism as having a poor sense of time. The authors modeled the data to provide a relative
assessment of ITS function in these individuals. The implications of these results for the
understanding of autism are discussed.

DOI: 10.1352/1944-7558-116.2.165

The ability to perceive the temporal proper- examining timing ability in these individuals,
ties of events and the temporal relations between there are not any studies (to our knowledge) that
them is fundamental for adaptive learning, have attempted to examine any correspondence
cognition, and behavior. Individuals are continu- between timing performance and autism symp-
ally timing events in their surrounding environ- tom severity. In the current study, we attempted
ment. The ability to estimate duration (which is to provide a preliminary assessment of the ability
shared by other species) and to use such temporal of individuals with autism to estimate duration (in
knowledge to mediate expectations and behavior the multiseconds range). We also took a ‘‘first
is at the core of adaptive function. Research has look’’ to see whether timing ability was predictive
revealed that distortions and perturbations in of diagnostic features of autistic disorder. We used
timing ability are present, to varying degrees, in methods that are well established in the study of
many patient populations and may accompany interval timing (e.g., see Allan & Gibbon, 1984).
differences in other aspects of sensory processing Although time is not a stimulus, the experi-
and cognitive and behavioral profiles. Recently ence of duration shares the same qualities as
research has suggested that differences in timing perception by other senses (e.g., vision, hearing)
and time perception might directly contribute to and is widely studied using a psychophysical
severity and features of autistic disorder (and the approach, which can be defined as an attempt to
triad of impairments; Allman & DeLeon, 2009; quantify the sensory response to physical stimuli
Boucher, 2001; Wimpory, 2002). Although to (see Gescheider, 1997). Accordingly, decades of
date there have been very few empirical studies basic interval timing research (in the seconds to

E American Association on Intellectual and Developmental Disabilities 165


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

minutes range) have revealed that the interval performance is usually comparable with adults
timing system (ITS) is likely to be made up of (temporal sensitivity improves between 3 and
various components (Gibbon, Church, & Meck, 8 years; e.g., Droit-Volet, Clément, & Wearden,
1984), with perceptual, memory, and decision 2001; Droit-Volet & Wearden, 2001). Behavioral
systems being involved. The ITS subserves our studies on the typical development of time
sensitivity to relatively short time scales, and, in perception in childhood serve a useful frame of
turn, adequate perception of duration is a key reference when comparing the performance of
component of adaptive cognitive, behavioral, and individuals with autism.
social functions. Sensitivity to time is also a basic If the typical development of the interval
building block of higher order notions of past, timing system is disturbed in autistic disorder,
present, and future (see Fraisse, 1982, 1984; several behavioral and cognitive profiles might be
Friedman, 1982), which form an intellectual expected to occur (see Allman & DeLeon, 2009;
structure for our everyday thoughts, intentions, Boucher, 2001). For example, if sensitivity to
and behavior. duration is reduced, infantile stereotyped behav-
Given the phylogenic generality of timing iors (e.g., hand flapping, body rocking) may
ability across species, it seems likely that the persist to facilitate the processing of duration
ability to estimate duration might emerge in early and effectively ‘‘count’’ time (Killeen & Fetter-
infancy. In fact, rhythmic changes in the seconds man, 1988; Skinner, 1948). Moreover, problems
to minutes range are inherent in many biological with timing and time perception may correspond
systems and repetitive movement patterns (e.g., to difficulties in acquiring language and interact-
breathing, sucking, stereotypies, and early vocal ing with the social environment, as timed
development such as crying and babbling; see coordination with others is fundamental for joint
Wolff, 1991). These repetitive actions and behav- attention, turn-taking, and social bonding (see
iors allow the infant to adapt to the temporal Wimpory, 2002). Language itself has inherent
contingencies of their physical and social envi- references to time (e.g., past, present, and future),
ronment (Pouthas, 1985). Throughout infancy, as do many executive functions (e.g., planning,
parent–infant interactions (including gaze and episodic memory).
vocalizations) follow exquisite temporal patterns, Two previous empirical reports that required
with the parent often rearranging his/her behavior individuals with autism to make a response or
to temporally match the infant, in ways that are temporal judgment that was accurately timed are
optimal for learning (e.g., see Jaffe, Beebe, relevant to the current study. Szelag, Kowalska,
Feldstein, Crown, & Jasnow, 2001). Furthermore, Galkowski, and Poppel (2004) required partici-
one of the so-called hallmark psychophysical pants to reproduce given durations (between
properties of interval timing, the scalar property— approximately 1–5 s) and observed quantifiable
the requirement that the standard deviation of and selective differences in the timed performance
time judgments is a constant fraction of the mean of individuals with autism. Unlike typically
judgment (this varies with the interval being developing participants who revealed a close
timed; Wearden & Lejeune, 2008)—was found in correspondence between the target and repro-
reciprocal parent–infant interactions (Stern, duced durations, those with autism displayed a
Beebe, Jaffe, & Bennett, 1977) and was observed tendency to reproduce all given durations around
in the brains of the youngest infants tested 3.0 to 3.5 s. In an equivalent study using adults
(6 months) during an interval timing task. In fact, with autistic disorder (Martin, Poirier, & Bowler,
a recent series of infant electroencephalography 2010), individuals with autism were less accurate
(EEG) studies (Brannon, Libertus, Meck, & in their temporal reproductions and more vari-
Woldorff, 2008; Brannon, Roussel, Meck, & able, particularly at longer durations (which
Woldorff, 2004) revealed that ability to time tended to be under-reproduced).
durations in the interval range further develops In the current study, we used a time
during infancy (i.e., there are quantifiable gains perception task that did not require a response
between 6 and 10 months of age). Beyond or temporal judgment to be accurately timed, to
infancy, there are somewhat inconsistent, but examine the ability of individuals with autistic
quantifiable, differences in the perception of disorder to estimate duration. We also simulated
interval durations across childhood (e.g., between our obtained data through a principled model
3 and 5 year olds), but by 8 years of age timing similar to the one applied to data reported from a

166 E American Association on Intellectual and Developmental Disabilities


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

large group of typically developing children with autism did not successfully acquire the
(Droit-Volet & Wearden, 2001), which used temporal discrimination (see Experimental Methods
methods almost identical to our own. The best section) and were withdrawn from the study.
fit of the model produces various parameters that As is common to many studies of temporal
represent functioning of different aspects of ITS bisection (e.g., Droit-Volet & Wearden, 2001;
(i.e., clock, memory, and decision stages). Second, Wearden, Wearden, & Rabbitt, 1997), only those
we administered a modified version of the It’s participants who produced orderly test data on
About Time questionnaire (Barkley, 1998, used both versions of the task were included in the
with permission; Barkley, Koplowitz, Anderson, final level of analysis (described later; 4 partici-
& McMurray, 1997), originally developed to pants with autism and 1 without autism produced
assess sense of time in children with attention- disorderly functions and were excluded from
deficit/hyperactivity disorder to parents of all further analysis). Data from 13 children with
individuals. autism and 12 comparison children who success-
fully completed both versions of the task are
reported in the current study. The characteristics
Method of individuals who constituted each group (autism
Participants or comparison) are presented in Table 1. Partic-
We recruited the majority of participants with ipants were not matched to each other by any
autism through existing research studies and the factors, although they represented a similar size
majority of those without autism via flyers posted and distribution in age across a large range (7–
around the pediatric facility and wider institution. 16 years; M age 5 10.3 years, Median 5 9 years,
The typically developing (comparison) group was per group). Although there were no statistical
a relative weakness of the current study because group differences for intelligence measures, only 3
only a few of these participants contributed (out of 12) comparison participants provided IQ
intelligence scores (due to the preliminary nature data, and these few comparison IQ scores tended
of the study, formal testing was not available), to be higher overall (see Table 1).
and, therefore, this group was particularly not well It is worth noting that the single previous
defined. Screening exclusion criteria for potential study that had related temporal bisection perfor-
comparison participants included a diagnosis of mance to IQ (Wearden et al., 1997) used typical
developmental, childhood, or psychiatric disorder adults (rather than children) but did not find any
and educational difficulties that were determined aspect of bisection performance that was affected
by parent interview (all procedures were approved by IQ, even though performance measures on
by the pertinent institutional review board). All other tasks were IQ dependent. There is no
participants were required to be free of any motor evidence in the literature that bisection perfor-
and/or visual impairment that would interfere mance differs according to gender, and the
with completion of task demands. All participants comparison group included 3 females.
in the autism group contributed diagnostic and
intelligence measures that had previously been Experimental Methods
administered by independent clinicians and We used a basic procedure known as temporal
researchers at the institution. All participants in bisection to examine the ability to estimate and
the autism group met the stringent autism cutoff discriminate durations in the seconds range. We
on both an observational assessment (Autism adapted methods previously used in a study of
Diagnostic Observation Schedule [ADOS]; Lord temporal bisection in typically developing chil-
et al., 2000) and parent interview (Autism dren (see Droit-Volet & Wearden, 2001, for
Diagnostic Interview—Revised [ADI-R]; Lord, additional procedural details). During the com-
Rutter, & LeCouteur, 1994), with the exception puterized procedure, individuals were initially
of 2 participants who met the cutoff for autism shown, then trained to discriminate between,
spectrum disorder on the observational assess- two anchor durations that were signaled by serial
ment (they also met criteria for autism on the presentations of the same visual stimulus (a rabbit
ADI-R). Thirty-two children, 19 individuals with or clown, for each of the two versions of the task)
autism and 13 comparison participants, were that appeared for the two standard times (initially
recruited into the study. Of these, 2 children identified as short and long by the experimenter

E American Association on Intellectual and Developmental Disabilities 167


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

Table 1. Participant Characteristics


Autism group (n 5 13; all males) Comparison group (n 5 12; 9 males)
Variable M SD Min.-max. M SD Min.-max.
Age (years) 10.3 2.4 7.3–15.2 10.3 3.1 7.3–16.8
FSIQ 92.31 17.13 72–118 109.80a 18.14a 78–122a
WISC IV only
WMIQ 92.13b 16.87b 56–107b
VCIQ 100.13b 27.34b 61–142b
PRI 116.13b 19.48b 79–141b
PSI 91.88b 12.91b 78–112b
ADOS (Mod 3)
Comm. 4.3c 2.17c 1–8c
RSI 8.69c 2.25c 4–13c
Comm.+ RSI 12.92c 3.81c 8–21c
SB/RI 2.54c 2.22c 0–7c
Total 15.46c 5.06c 8.25c
ADI-R
A 21.62 5.39 13–28
B 17 3.97 10–23
C 6.92 2.50 3–11
D 4.08 .95 3–5
Note. FSIQ 5 Full scale intelligence quotient; WISC; Wechsler Intelligence Scale for Children, Version 4 (Wechsler,
2004); WMIQ 5 working memory IQ; VCIQ 5 verbal comprehension IQ; PRI 5 perceptual reasoning IQ; PSI 5
processing speed index; ADOS 5 Autism Diagnostic Observation Schedule (Lord et al., 2000); Mod 5 module; Comm 5
communication; RSI 5 reciprocal social interaction; SB/RI 5 stereotyped behavior/restricted interests; Total 5 (Comm.
+ RSI) + (SB/RI); ADI-R: 5 Autism Diagnostic Interview—Revised (Lord, Rutter, & LeCouteur, 1994); A 5 language and
communication; B 5 social interaction; C 5 repetitive behaviors; D 5 onset of symptoms before 36 months.
a
n 5 3. b n 5 8. c n 5 11 values denote the number of participants for whom scores were available (see text for details).

sitting next to them). Participants were required to or wrong now, but you need to decide if you think
classify a temporal judgment as either short or it is it more like the short one, or more like the
long by selecting between two different response long one’’). Five intermediate durations and the
options (e.g., two different buttons). The S and L two anchors were each presented four times in an
keys on the laptop keyboard were each covered intermixed block (without feedback). Two test
with a yellow, colored sticker with ‘‘S-’’ and ‘‘L—’’ blocks were typically presented (with a short break
printed on it (these keys are on the central row to in the testing room between each).
the left and right, respectively) and were the short During experimental testing, the accompany-
and long choice options. Whether the response ing caregiver was required to complete the It’s
was correct was signaled by computer feedback About Time questionnaire (Barkley, 1998) in a
(and by the experimenter). After meeting an separate area.
accuracy criterion (seven of eight correct respons-
es in one block, up to six blocks) and a short break Arrangement of Timing Events
in the testing room, participants were presented All participants completed two versions of the
with a new set of stimulus durations that were same task, in a counterbalanced order with respect
between the two anchors and were required to to group allocation. A 20-min break with the
make a judgment about a given duration’s accompanying caregiver was interleaved (in a
‘‘similarity’’ to the short or long anchor (they playroom equipped with a television and toys
were instructed, ‘‘You might find it a bit harder to and with the opportunity to leave and get a
decide and you won’t find out if you got it correct snack). The two versions differed with respect to

168 E American Association on Intellectual and Developmental Disabilities


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

the objective length of the pairs of anchor (and curves, linear regression, interpolation by eye) that
intermediate) durations used, with one being yielded very similar results; therefore, we averaged
shorter and the other longer. In the shorter across them (these constitute the BP and WR data;
version of the task, the anchor durations were 1 see also Wearden & Ferrara, 1995). Data from
and 4 s (intermediates durations 5 1.5, 2, 2.5, 3, participants with and without autism were then
and 3.5 s), and in the longer version the anchors compared and averaged to produce the group mean
were 2 and 8 s (intermediates durations 5 3, 4, 5, (to examine any group BP and WR differences).
6, and 7 s). We assumed these versions were The scalar property was further assessed by plotting
equivalent in discrimination difficulty due to the group data obtained with two different duration
1:4 ratios between the respective anchor pairs. ranges on the same relative scale, and we expected
After the presentation of a given stimulus them to superimpose perfectly (so it looks as
duration, the words Which Time? appeared on though only one function is present; this is often
the screen, and a response (short or long) could be found in animal and human timing studies).
recorded. If no response was made within a 10-s
period, the trial repeated (the duration was Computer Modeling
presented again). The interval between the end The same principled model (Wearden, 1991)
of one trial and the start of the next trial, denoted that was applied to the data from typically
by a small fixation cross on the screen, was varied developing children in a previous study (Droit-
between 1 s and 5 s. Testing could be paused Volet & Wearden, 2001) was applied to our
during the intertrial interval (ITI; e.g., to correct obtained group data. This treatment allowed us to
any off-task behavior). make direct comparisons between the timing of
individuals with autism with different age groups
Psychophysical Performance Measures of typically developing children outside of the
The proportion of long responses (denoted as current study (which was particularly useful given
pLong) produced at each test duration was calcu- the limitations with our comparison group).
lated for each individual, on each separate version Because the model attempted to simulate timing
of the task. This was achieved for a given duration, performance, in doing so it made two assump-
by dividing the number of long responses to the tions: First, there was the assumption that the
sum of short and long responses. To be considered choice to respond (short or long) to any of the test
‘‘orderly,’’ the pLong responses were required to durations was governed by the smaller of the two
generally increase with objective duration. These differences between a given test duration and the
individual pLong values then contributed to the remembered short and long trained anchors (1
group mean functions (shown in Figure 1). and 4 s, or 2 and 8 s). The second assumption was
A given individual’s timing functions are that the anchor durations may have been
referred to as psychophysical functions, because they remembered incorrectly as shorter or longer than
allow extrapolation and quantification of indexes of they really were (see Droit-Volet et al., 2001;
timing sensitivity and ability: The duration that Meck, 1983, for applications of this idea), and this
produces 50% pLong responses (when the individ- ‘‘effective’’ value was used for the difference
ual is equally likely to classify the duration as short comparison during the test stage. The model
or long) is known as the bisection point (BP). In derives various indexes of performance (K*, c),
human timing, the BP is usually located around the much like the ones derived from the psychophys-
arithmetic mean of the two anchor standards ical functions themselves, although these corre-
(Wearden, 1991); temporal variability is indexed sponded to temporal memory distortion (K*) and
by the difference limen (DL; half of the difference timing sensitivity (c). For example, if K* equals 1,
between 75% and 25% pLong divided by the BP); then the anchors are stored as their real values; if
and temporal sensitivity is indexed by the Weber K* is less than 1, the anchors are remembered as
ratio (WR), which is also used to assess the hallmark shorter; and if K* is greater than 1, they are
scalar property of timing (DL divided by BP). As remember as longer than they really were (e.g., if
WR values are thus normalized, temporal sensitiv- K* 5 .95, the anchors are remembered as 95% of
ity across a range of pair durations can be reliably the real values). For each version of the task, 1,000
compared. These measures were derived for all trials were simulated at each of the seven test
individuals, by three different methods (logistic durations, and K* and c were varied to produce

E American Association on Intellectual and Developmental Disabilities 169


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

the best fit of the model, represented by the mean participant who produced disorderly data was the
absolute deviation value (MAD; the sum of the youngest in the group). There were no obvious
absolute deviations divided by 7, the number of characteristics of these individuals with respect to
data points) between the model’s output and the diagnostic or intelligence scores, and, given our
data point for each condition. Small MAD values relatively small sample size, the current study was
indicate a good fit, and the MAD values in this too limited in scope to speculate on what
study could be classified as good in the wider individual differences made it difficult for some
literature. The lines in Figure 1 show the fit of the individuals to complete the task.
model to the obtained data.
Performance on the Time Perception Task
Results Across both versions of the task, individuals
with autism produced a greater proportion of
Training pLong responses compared with those without
The training performance of those partici- autism. In the 1- versus 4-s (shorter) version of the
pants with and without autism did not differ task, analysis of variance (ANOVA) with two
between groups, with respect to the number of between-subjects factors, group and task order,
training blocks required to successfully acquire and a within-subject factor of stimulus duration
the discrimination, in both versions of the task revealed a significant effect of group, F(1, 21) 5
( ps . .5). However, this does not preclude the 4.62, p , .05; no effect of order, F(1, 21) 5 1.64,
possibility of differences in how participants in p 5 .22; an effect of duration, F(6, 126) 5 90.63,
each group acquired the task. No participants p , .001; and no significant interactions between
demonstrated or subsequently reported counting these factors (largest F 5 1.77). Planned compar-
during timing (see also Droit-Volet & Wearden, isons revealed a significant group difference at the
2001). Two participants with autism displayed 3.5-s duration, F(1, 21) 5 10.51, p 5 .003. In the
interesting features during timing, however. One 2- versus 8-s (longer) version of the task, an
individual put his fingers together and then pulled ANOVA with the same factors revealed no effect
them apart during the training stage, particularly of group or order (ps . .1) and an effect of
to longer durations, and continued to do this duration, F(6, 126) 5 104.42, p , .001. There was
during a small proportion of test trials, and also a significant interaction between group and
another individual (relatively higher functioning) duration, F(1, 21) 5 3.93, p 5 .010, but no other
reported that, ‘‘If my mind turns over once its significant interactions (largest F 5 1.44, p 5
short, and more than once its long’’ (he reported .206). Planned comparisons revealed group differ-
seeing a visual snake in his mind, which rotated). ences at the 4-s, F(1, 21) 5 4.40, p , .05, and 5-s
Unfortunately, a coding observer was not present durations, F(1, 21) 5 6.66, p 5 .02.
and experimental sessions were not videotaped, so Figure 1 shows (empty and filled circles) that,
the possibility of conducting additional observa- in both the shorter and longer versions of the task
tional analyses of behaviors during timing was not (upper and lower panels, respectively), the ob-
possible in the current study. tained group timing functions from individuals
Individuals who could not acquire the with autism were shifted to the left, relative to the
discrimination (i.e., did not complete the test comparison group functions. Furthermore, in the
phase) and those individuals who acquired the 2- versus 8-s version of the task (lower panel), the
discrimination but produced disorderly timing autism group function is relatively flat to durations
functions (i.e., did not contribute data) tended to above about 5 s. (i.e., the empty circles are on a
have autism: Two participants failed to acquire flatter plane). Across both versions, therefore,
the initial discrimination, and both had autism. individuals with autism exhibited a greater propor-
Five participants produced disorderly data and tion of pLong responses and produced somewhat
were excluded from final analysis; 4 had autism. leftward-shifted timing functions; they also began
Participants with autism who did not successfully to show potentially interesting differences in the
acquire the discrimination were at the minimum perception of durations over 3.5–5.0 s (relative to
of the group age range (,7 years), but those who comparison individuals). The overall shape of the
produced disorderly functions spanned the full two timing functions produced by the comparison
age range (up to 17 years; the typically developing group was normal, especially in the longer version;

170 E American Association on Intellectual and Developmental Disabilities


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

BP 5 4.34, comparison group’s BP 5 5.05; z 5


22.01, p , .05, respectively). However, our
comparison group produced a BP that was higher
than would be normally expected in the 1- versus
4-s version of the task, and this contributed to the
group difference (the comparison BP was typical
in the 2- vs. 8-s version). In addition, for any given
individual, we should expect to observe a
reasonable difference between the two BPs for
each version, as the two pairs of anchor durations
we used differed. Close inspection of individual
timing functions for all individuals showed that
the majority of participants with autism did not
have the extent of expected difference between
the location of the BP across both versions of the
task, but the majority of comparison participants
displayed this expected difference (W. H. Meck,
personal communication, April 2010).
As depicted in the lower panels of Figure 2,
there were no group differences in the sensitivity
to duration (WR) when the anchors were 1 and 4 s
(autism group’s WR 5 .18; comparison group’s
WR 5 .21, p . .25). However, in the longer
version of the task, the WR was significantly
higher for the group with autism, indicating
‘‘worse’’ temporal sensitivity when the anchor
durations were 2 and 8 s (autism group’s WR 5
.26, control group’s WR 5 .18, z 5 21.96, p 5
.05). Both of the WR values for the comparison
group (and the autism group WR on the shorter
version of the task) were similar to those usually
Figure 1. Data points (empty and filled circles) obtained with typically developing children
and best fitting values from the model described (8 years old); however, the autism WR in the
in the text (dashed and solid lines) from longer version of the task was comparable with
participants with and without autism (respective- that obtained with typically developing 3–5 year
ly), in both versions of the task (upper panel: 1 vs. old children (see Droit-Volet & Wearden, 2001).
4 s discrimination; lower panel: 2 vs. 8 s The two timing functions produced by each
discrimination). Compar. 5 comparison group. group (one for each version of the task) were also
subjected to the test of superimposition to assess
the presence of the hallmark scalar property of
although in the shorter version of the task, the interval timing (see Droit-Volet & Wearden, 2001,
function was slightly rightward shifted. for details on how this is done). As shown in
Figure 3, the two timing functions from the
Psychophysical Measures comparison group superimposed perfectly, and,
Figure 2 reveals the group distribution of the for those with autism, the group functions
two derived psychophysical indexes on the shorter superimposed to a lesser extent but still reason-
(left-hand panels) and longer (right-hand panels) ably well (somewhat comparable with 3 year olds;
versions of the task. As depicted in the upper row Droit-Volet & Wearden, 2001). Our data were
of panels, the autism group’s BP was located at a equivocal as to whether the scalar property was
significantly shorter duration, on both versions of found in the timing of individuals with autism,
the task, compared with those without autism and it would be of potential future interest to
(autism group’s BP 5 2.5; comparison group’s BP examine whether scalar timing patterns are found
5 2.98; z 5 22.34, p , .02; and autism group’s in aspects of communication, social reciprocity,

E American Association on Intellectual and Developmental Disabilities 171


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

Figure 2. Derived individual values for participants with and without autism of the bisection point
(upper panels) and Weber ratio (lower panels), on both versions of the task (left panels: 1 vs. 4 s; right
panels: 2 vs. 8 s).

and repetitive behaviors in individuals with autistic behaviors; and total IQ and specific domain
disorder. scores for processing speed, working memory,
As an additional level of analysis, we exam- verbal comprehension, and perceptual reasoning.
ined relationships between the psychophysical Pearson product-moment correlations revealed a
timing indexes (BP and WR) and diagnostic and correspondence between BP in the 1- versus 4-s
intelligence measures of our participants with (shorter) version of the task with the score for
autism (this type of analysis was not performed for language and communication (ADOS) and score
comparison participants). Only those participants for working memory (BP with communication:
who were previously administered the Module 3 r 5 2.641; p 5 .033; BP with working memory:
ADOS (Lord et al., 2000), and contributed r 5 .763, p 5 .028; communication and working
Wechsler Intelligence Scale for Children, Fourth memory: r 5 2.793; p 5 .019). That is, the
Edition (WISC-IV; Wechsler, 2004) intelligence shorter the location was of the BP, the ‘‘poorer’’
scores were used in this level of analysis (see an individual’s language and communication and
Table 1 note). We examined BP and WR working memory was. (Total IQ score was not
(sensitivity) scores for each version of the task; predictive of timing measures or diagnostic
diagnostic scores (ADOS and ADI-R [Lord et al., scores.) Close examination of the individual
2000, 1994]) for language and communication, timing functions produced by the few individuals
social interaction, and restricted and repetitive with autism who had the lowest scores for

172 E American Association on Intellectual and Developmental Disabilities


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

(.50 and .53, respectively) compared with those


without autism (.42 and .37, respectively), sug-
gesting more variable (i.e., ‘‘fuzzy’’) temporal
reference memories. The values obtained for the
autism group were comparable with those previ-
ously reported using typically developing 5 year
olds, and our comparison group values were
consistent with those from older children (8 years
old; see Droit-Volet & Wearden, 2001). The
second parameter from the model that provides
an index of memory distortion for the anchor
pairs, revealed that both groups produced K*
values (autism group 5 0.97; comparison group
51.17) similar to those previously obtained with
typically developing children (8 years old) when
the anchor durations were 1 s and 4 s. However,
although this was also true for the comparison
group when the anchors were 2 s and 8 s (K* 5
0.98), the autism group produced a lower value
(K* 5 0.83), suggesting a tendency to shorten the
memory of the anchors on the longer version of
the task to an extent that was comparable with
typically developing 3 year olds (on a task of
temporal generalization, Droit-Volet, Clément, &
Wearden, 2001). Results from the modeling lend
support to the idea that timing ability may be
developmentally delayed in individuals with
autistic disorder.

Figure 3. Obtained group data plotted on the Findings From the Parental Time Questionnaire
same relative scale for participants with (upper Table 2 displays sample questions and scoring
panel) and without (lower panel) autism. on this instrument (which was modified slightly
from its original version). The maximum score on
communication and working memory (and, the adjusted questionnaire is 75 (best) and the
hence, the shorter BP when the anchors were 1 s minimum is 0 (worst). The mean score for
and 4 s) revealed that they tended to display a participants with autism (18.08; range 5 6–37)
protracted flattening in their timing functions to was significantly lower than for comparison
durations over 2 s (in the 1- vs. 4-s version). At a participants (48.4; range 5 31–73), t(21) 5
more general level, it is striking that inspection of 26.12, p 5 .001. Parental responses to the final
all individual timing functions produced by question (No. 25), ‘‘In general, compared to other
participants with autism when the anchor dura- children of their age, how well developed is your
tions were 2 s and 8 s revealed that almost 70% (9 child’s sense of time?’’, revealed a group differ-
out of 13 participants) displayed characteristic ence, t(21) 5 25.38, p 5 .001, with the modal
flattening to durations over 5 s—of the 4 answer for participants with autism being poor
participants with autism who did not show this compared with above average for the comparison
unusual pattern, 3 shared the highest group scores group (scale: poor [0], below average, average, above
for working memory. average, well above average [4]). Based on previous
reports (Boucher, Pons, Lind, & Williams, 2007)
Parameters From Computer Modeling of problems with diachronic thought (i.e., affected
The indexes derived from the modeling reveal individuals are less likely to think about past or
that in both the shorter and longer versions of the future stages of a current situation; have difficulty
task, individuals with autism had higher c values understanding that things can change or evolve

E American Association on Intellectual and Developmental Disabilities 173


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

Table 2. Example Questions as They Related to Past, Current, and Future Time Referencea
Past Managing current time Future
How often does your child When working on a task, how How often does your child talk
ask questions about their often does your child seem about or seem to think about
past? to get work done in time what he/she will be doing
allotted? tomorrow?
How often does your child How often does your child How often does your child
seem to think about their refer to a watch or clock in consider the future
past or use hindsight before planning how much time he or consequences of their
responding to a situation? she has left to do something? actions for him/herself?
Note. Scoring is typically as follows: rarely (0), sometimes (1), most of the time (2), and almost always (3).
Taken from the ‘‘It’s About Time’’ questionnaire. Copyright R. A. Barkley, 1998. Reprinted with permission.
a

over time but remain the same; and that and WR) revealed significant and potentially
successive states or events are part of a unitary characteristic differences in bisection performance
whole) in autism, we also arbitrarily categorized and suggest that individuals with autism experi-
the questions (with the exception of No. 25) enced greater difficulty discriminating between
according to past, managing current time, or future longer durations.
(see Table 2) and reported group differences for BP values were correlated with language and
each type, smallest t(11) 5 23.308, p , .004. communication, as well as working memory
When interpreting these findings, it is useful to scores in the shorter version of the task.
note that this questionnaire is not tailored to Computer modeling suggested that individuals
compensate for known problems with communi- with autism appeared to have more variable
cation and socialization in children with autism temporal memories (c) and were likely to truncate
and cannot disentangle the assessment of time the anchor durations when they were 2 s and 8 s
from other executive functions, nor can our (K*). Additional comparisons with other child-
rudimentary classification of managing current hood studies suggest the extent of these differ-
time, which included time frames that spanned ences may be of some developmental significance.
many minutes and hours. Last, parents of children with autism tended to
classify their children as having a qualitatively
poor sense of time, which attests to the many
Discussion
anecdotal reports that these individuals experi-
To our knowledge, the current study repre- ence difficulties with time (see Allman & DeLeon,
sents the first attempt to examine the perception 2009; Boucher, 2001).
of multisecond durations in individuals with Some interesting features of the data are also
autistic disorder. The study was preliminary in consistent across various levels of analysis and
nature and has some notable strengths (the strengthen the assertions that can be made,
psychophysical method and modeling of data) despite the limitations in scope. In particular, it
and weaknesses (the inadequate characterization appears that individuals with autism experience
of the comparison group and small sample size). difficulties with durations exceeding about 3.5 s to
The extent of our different levels of analysis 5.0 s and may be less able to discriminate between
allows us to make a variety of claims about longer durations (likely related to poorer temporal
performance and the experience of duration for sensitivity). The question then becomes: How
individuals with autistic disorder. Individuals with might a problem experiencing longer durations
autism tended to produce a greater proportion of influence test performance and produce the
long responses and displayed a relatively robust variety of measures obtained? There are at least
flattening in their timing functions, particularly to two possibilities. First, it is possible that both the
durations exceeding about 5 s (that did not result short and long anchor standard durations influ-
from a failure of experimental control). Psycho- enced bisection performance in the shorter, 1-
physical measures for individuals with autism (BP versus 4-s version, but a different strategy was used

174 E American Association on Intellectual and Developmental Disabilities


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

in the longer, 2 versus 8-s version. When the may have difficulty with durations beyond the
anchors were 2 s and 8 s, the short anchor (2 s) bounds of the psychological present. The weak
may have had a stronger influence over test central coherence hypothesis of autism (Frith,
performance than the long anchor (8 s). This 1989; Happé, 1999) and reported deficits in the
account requires some form of psychological temporal binding of stimulus input in autistic
explanation for why those with autism appear to disorder (e.g., Bebko, Weiss, Demark, & Gomez,
be less influenced by the memory of the longest 2006; Brock, Brown, Boucher, & Rippon, 2002)
standard. Of course, this could have been due to might be related to problems linking successive
difficulty maintaining attention, concentration, or periods or platforms together. There is recent
(which leads us onto the second possible expla- evidence that individuals with autism integrate
nation for the two key findings [BP differences sensory input over an extended temporal window
and the relative flattening]) there may have been (Foss-Feig et al., 2010) and experience difficulties
some underlying difficulty with, or insensitivity grasping the concept of time and regulating and
to, longer durations (e.g., ‘‘time blindness’’), structuring their behavior and expectations within
particularly those over 3.5 s to 5.0 s in autistic current and future imagined time frames (Bou-
disorder. cher, 2001; Boucher et al., 2007).
In fact, this 3.5–5.0-s period is not altogether A complication of the multiprocess nature of
arbitrary, as it is widely held to correspond to the the ITS is that the development of psychological
specious or psychological present. The idea of such a variables other than timing ability, such as
putative mental platform has been posited since differences in attention and memory and decision
the dawn of psychology (James, 1890), and it is ability, may also play a role in timing performance
held to facilitate linking together sensory experi- (e.g., Lustig, Matell, & Meck, 2005). For example,
ences close together in time. The temporal the temporal limit of short-term (or immediate)
breadth of this platform (although not fixed) is memory is only a few seconds (Block, 1979), but
believed to be around 3 s to 5 s (possibly up to 8 s; temporal constraints are somewhat longer for
e.g., see Block, 1990; Fraisse, 1984; Michon, 1978; working memory (several seconds; Baddeley &
Poppel, 1997) and has been studied under a Hitch, 1974).
variety of experimental paradigms. These include In many ways, the results of the current study
the temporal segmentation of spontaneous create many more questions than they answer,
speech, structuring a continuous stream of and, given the preliminary nature of the study and
auditory input, programming anticipatory move- its limitations, the findings should be treated with
ment, and sensorimotor behavior (see Poppel, some caution. They will need to be replicated
1997). This platform can be considered intimately with at least double the number of participants
related to the perception of the durations used in and extended under a wide range of different
both versions of our task. In accounting for their temporal parameters before any reliable assess-
observation that individuals with autism tended ment of timing ability in autistic disorder can be
to reproduce given durations that ranged between made (ongoing research by the first author
about 1 s and 5 s (around 3.0–3.5 s), Szelag et al. [M.A.]). In addition, the autism group likely
(2004) suggested that the processing of duration included different subgroups of affected individ-
was dissociated from the temporal platform and uals (i.e., some of whom had phrase speech and,
that autism involved a unique form of timing so, completed the Module 2 ADOS, whereas
disturbance. In the current study, we extended the others had fluent speech), and this limits the
generality of these findings by revealing that generality of our findings. It may be particularly
individuals with autism appear able to discrimi- useful for future studies to examine timing ability
nate and perceive durations within the bounds of in high-functioning individuals with autism, and
the psychological present (up to about 5 s), unless those who are less verbal. Nevertheless, the
they have poor communication or working strengths of our psychophysical approach allow
memory, in which case they may experience us to make some intriguing observations about
problems for durations within the bounds of the the timing functions of individuals with autism,
temporal platform (see also Mostofsky, Goldberg, and some meaningful comparisons with previous
Landa, & Denckla, 2000, who reported no studies that used different age groups of typically
differences in autism when discriminating milli- developing children. At the very least, we have
second intervals between stimuli). However, they demonstrated the benefit of using this approach

E American Association on Intellectual and Developmental Disabilities 175


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

with children with autistic disorder. Undoubtedly, Block, R. A. (1990). Models of psychological time.
the potential benefit of continuing this relatively In R. A. Block (Ed.), Cognitive models of
new line of investigation is to inform related psychological time (pp. 1–35). Hillsdale, NJ:
avenues of cognitive and behavioral autism Erlbaum.
research (e.g., joint attention, social timing), both Boucher, J. (2001). ‘‘Lost in a sea of time’’: Time-
at the basic and applied levels, and to improve parsing and autism. In C. Hoerl & T.
clinical outcomes. For example, temporal vari- McCormack (Eds.), Time and memory (pp.
ables are often a core aspect of clinical and 111–135). Oxford, United Kingdom: Oxford
educational training and treatment programs (e.g., University Press.
operant reinforcement schedules, timetables, and Boucher, J., Pons, F., Lind, S., & Williams, D.
time-out), and these might be advanced by (2007). Temporal cognition in children with
increased awareness of temporal experience in autistic spectrum disorders: Tests of diachron-
autistic disorder (see Critchfield & Kollins, 2001; ic thinking. Journal of Autism and Developmen-
Lalli, Casey, Goh, & Merlino, 1994; MacDuff, tal Disorders, 37, 1413–1429.
Krantz, & McClannahan, 1993). To the extent Brannon, E. M., Libertus, M. E., Meck, W. H., &
that the neurobiological basis of (typical) interval Woldorff, M. G. (2008). Electropsychological
timing is beginning to be elucidated (e.g., Buhusi measures of time processing in infant and
& Meck, 2005; Meck, 2003), an improved adult brains: Weber’s law holds. Journal of
understanding of the neurobiological basis of Cognitive Neuroscience, 20, 193–203.
timing in autistic disorder may be particularly Brannon, E. M., Roussel, L. W., Meck, W. H., &
informative with regard to potential pharmaco- Woldorff, M. (2004). Timing in the baby
logical remediation. brain. Cognitive Brain Research, 21, 227–233.
Brock, J., Brown, C. C., Boucher, J., & Rippon, G.
(2002). The temporal binding deficit hypoth-
References esis of autism. Development and Psychopatholo-
Allman, M. J., & DeLeon (2009). No time like the gy, 14, 209–224.
present: Time perception in autism. In A.C. Buhusi, C. V., & Meck, W. H. (2005).What makes
Giordano & V.A. Lombardi (Eds.), Causes and us tick? Functional and neural mechanisms of
risks for autism (pp. 65–76). New York: Nova interval timing. Nature Reviews Neuroscience, 6,
Science. 755–765.
Baddeley, A. D., & Hitch, G. (1974). Working Critchfield, T. S., & Kollins, S. H. (2001).
memory. In G. H. Bower (Ed.), The psychology Temporal discounting: Basic research and
of learning and motivation (Vol. 8., pp. 47–89). the analysis of socially important behavior.
New York: Academic Press. Journal of Applied Behavior Analysis, 34, 101–
Barkley, R. A. (1998). It’s About Time Question- 122.
naire. Syracuse, NY: Author. Droit-Volet, S., Clément, A., & Wearden, J. H.
Barkley, R. A., Koplowitz, S., Anderson, T., & (2001). Temporal generalization in 3- to 8-
McMurray, M. B. (1997). Sense of time in year-old children. Journal of Experimental Child
children with ADHD: Effects of duration, Psychology, 80, 271–288.
distraction and stimulant medication. Journal Droit-Volet, S., & Wearden, J. H. (2001).Tempo-
of the International Neuropsychological Society, 3, ral bisection in children. Journal of Experimen-
359–369. tal Child Psychology, 80, 142–159.
Bebko, J. M., Weiss, J. A., Demark, J. L., & Foss-Feig, J. H., Kwakye, L. D., Cascio, C. J.,
Gomez, P. (2006). Discrimination of temporal Burnette, C. P., Kadivar, H., Stone, W. L. &
synchrony in intermodal events by children Wallace, M. T. (2010). An extended multi-
with autism and children with developmental sensory temporal binding window in autism
disabilities without autism. Journal of Child spectrum disorder. Experimental Brain Re-
Psychology and Psychiatry, 47, 88–98. search, 203, 381–389.
Block, R. A. (1979). Time and consciousness. In Fraisse, P. (1982). The adaptation of the child to
G. Underwood & R. Stevens (Eds.), Aspects of time. In J. W. Friedman (Ed.), The develop-
consciousness: Vol. 1. Psychological issues (pp. mental psychology of time (pp. 113–140). New
179–217). London: Academic Press. York: Academic Press.

176 E American Association on Intellectual and Developmental Disabilities


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

Fraisse, P. (1984). Perception and estimation of MacDuff, G. S., Krantz, P. J., & McClannahan, L.
time. Annual Review of Psychology, 35, 1–36. E. (1993). Teaching children with autism to
Friedman, W. J. (1982). Introduction. In W. J. use photographic activity schedules: Mainte-
Friedman (Ed.). The developmental psychology of nance and generalization of complex response
time (pp. 1–11). New York: Academic Press. chains. Journal of Applied Behavior Analysis,
Frith, U. (1989). Autism: Explaining the enigma. 26, 89–97.
Oxford, United Kingdom: Blackwell. Martin, J. S., Poirier, M., & Bowler, D. M. (2009).
Gescheider, G. A. (1997). Psychophysics: The Brief report: Impaired temporal reproduction
fundamentals. Mahwah, NJ: Erlbaum. performance in adults with autism spectrum
Gibbon, J., & Allan, L. (Eds.). (1984). Timing and disorder. Journal of Autism and Developmental
time perception (Annals of the New York Disorders, 40, 640–646.
Academy of Sciences, Vol. 423). New York: Meck, W. H. (1983). Selective adjustment of the
New York Academy of Sciences. internal clock and memory processes. Journal
Gibbon, J., Church, R. M., & Meck, W. H. (1984). of Experimental Psychology: Animal Behavior
Scalar timing in memory (Annals of the New Processes, 9, 171–201.
York Academy of Sciences, Vol. 423). In J. Meck, W. H. (2003). Functional and neural
Gibbon & L. Allen (Eds.), Timing and time mechanisms of interval timing. Boca Raton,
perception (pp. 52–77). New York: New York FL: CRC Press.
Academy of Sciences. Michon, J. A. (1978). The making of the present.
Happé, F. G. E. (1999). Autism: Cognitive deficit In J. Requin (Ed.), Attention and performance
or cognitive style? Trends in Cognitive Sciences, (pp. 90–111). Hillsdale, NJ: Erlbaum.
3, 216–222. Mostofsky, S. H., Goldberg, M. C., Landa, R. J., &
Jaffe, J., Beebe, B., Feldstein, S., Crown, C., & Denckla, M. B. (2000). Evidence for a deficit
Jasnow, M. (2001). Rhythms of dialogue in in procedural learning in children and ado-
infancy. Monographs of the Society for Research
lescents with autism: Implications for cere-
in Child Development, 66(2 Serial No. 265).
bellar contribution. Journal of International
James, W. (1890). The principles of psychology (Vol.
Neuropsychological Society, 6, 752–759.
1., pp. 605–642). New York: Holt.
Poppel, E. (1997). A hierarchical model of
Killeen, P. R., & Fetterman, J. G. (1988). A
temporal perception. Trends in Cognitive
behavioral theory of timing. Psychological
Neuroscience, 1, 56–61.
Review, 95, 274–295.
Lalli, J. S., Casey, S., Goh, H., & Merlino, J. Pouthas, V. (1985). Timing behavior in young
(1994). Treatment of escape-maintained aber- children: A developmental approach to con-
rant behavior with escape extinction and ditioned spaced responding. In J. A. Michon
predictable routines. Journal of Applied Behav- & J. L. Jackson (Eds.), Time, mind and behavior
ior Analysis, 27, 705–714. (pp. 100–109). New York: Springer-Verlag.
Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Skinner, B. F. (1948). ‘‘Superstition’’ in the
Leventhal, B. L., DiLavore, P. C., et al. (2000). pigeon. Journal of Experimental Psychology, 38,
The Autism Diagnostic Observation Sched- 168–172.
ule—Generic: A standard measure of social Stern, D. N., Beebe, B., Jaffe, J., & Bennett, S. L.
and communication deficits associated with (1977). The infant’s stimulus world during
the spectrum of autism. Journal of Autism and social interaction: A study of caregiver
Developmental Disorders, 30, 205–223. behaviors with particular reference to repeti-
Lord, C., Rutter, M., & LeCouteur, A. (1994). tion and timing. In H. R. Schaffer (Ed.),
Autism Diagnostic Interview—Revised: A re- Studies in mother-infant interaction (pp. 177–
vised version of a diagnostic interview for 202). London: Academic Press.
caregivers of individuals with possible perva- Szelag, E., Kowalska, J., Galkowski, T., & Poppel,
sive developmental disorders. Journal of Au- E. (2004). Temporal processing deficits in
tism and Developmental Disorders, 24, 659–685. high-functioning children with autism. British
Lustig, C., Matell, M. S., & Meck, W. H. (2005). Journal of Psychology, 95, 269–282.
Not ‘‘just’’ a coincidence: Frontal-striatal Wearden, J. H. (1991). Human performance on an
interactions in working memory and interval analogue of an interval bisection task. Quarterly
timing. Memory, 13, 441–448. Journal of Experimental Psychology, 43B, 59–81.

E American Association on Intellectual and Developmental Disabilities 177


VOLUME 116, NUMBER 2: 165–178 | MARCH 2011 AJIDD

Time perception in autism M. J. Allman et al.

Wearden, J. H. (2001). Internal clocks and the Wolff, P. H. (1991). Endogenous motor rhythms
representation of time. In C. Hoerl & T. in young infants. In J. Fagard & P. H. Wolff
McCormack (Eds.), Time and memory (pp. 37– (Eds.), The development of timing control and
58). Oxford, United Kingdom: Clarendon temporal organization in coordinated action
Press. (advances in psychology) (Vol. 81, pp. 119–
Wearden, J. H., & Ferrara, A. (1995). Stimulus 133). Amsterdam: Elsevier.
spacing effects in temporal bisection by
humans. Quarterly Journal of Experimental
Psychology, 48B, 289–310. Received 6/18/2009, accepted 10/31/2010.
Wearden, J. H., & Lejeune, H. (2008). Scalar Editor-in-Charge: Leonard Abbeduto
properties in human timing: Conformity and
violations. Quarterly Journal of Experimental This work was supported in part by a Eunice
Psychology, 61, 569–587. Kennedy Shriver National Institute of Child
Wearden, J. H., Wearden, A. J., & Rabbitt, P. M. Health & Human Development career develop-
A. (1997). Age and IQ effects on stimulus ment award (Pathway to Independence) to Melissa
response timing. Journal of Experimental Psy- J. Allman (Grant K99 HD058698). A portion of
chology: Human Perception and Performance, 23, these data were presented at the annual meeting of
962–979. the Association for Behavior Analysis (2009) and
Wechsler, D. (2004). The Wechsler Intelligence Society for Neuroscience (2008). Correspondence
Scale for Children—Fourth edition. London: regarding this article should be sent to Melissa J.
Pearson Assessment. Allman, Johns Hopkins University School of
Wimpory, D. (2002). Social timing, clock genes Medicine and Kennedy Krieger Institute, 707
and autism: A new hypothesis. Journal of N. Broadway, Baltimore, MD 21205. E-mail:
Intellectual Disability Research, 46, 352–358. allman@kennedykrieger.org

178 E American Association on Intellectual and Developmental Disabilities

You might also like