Atypical development of motion processing trajectories in children with autism
Dagmara Annaz1 ,3 Anna Remington,1 Elizabeth Milne2, Mike Coleman1, Ruth Campbell1 Michael Thomas3, and John Swettenham1
1
Department of Developmental Sciences, Division of Psychology and Language
Science, University College London, UK 2 3
Department of Psychology, University of Sheffield, UK Developmental Neurocognition Lab, Birkbeck, University of London, UK
1 Developmental
Sciences, Division of Psychology and Language Science University College London, Chandler House, 2 Wakefiled Street, London WC1N 1PF, UK.; e-mail:
[email protected] 3
Developmental Neurocognition Laboratory, Birkbeck University of London, Malet Street, London, WC1E 7HX, UK.; e-mail:
[email protected]
Abstract Recent findings suggest that children with autism may be impaired in the perception of biological motion from moving point-light displays. There have also been reports that some children with autism have abnormally high motion coherence thresholds. In the current study we tested a group of children with autism and a group of typically developing children aged 5 to 12 years of age on three different motion perception tasks: i) biological motion, ii) motion coherence and iii) form-from-motion, as well as a static perception task iv) contour integration. Our aims were to examine the specificity of any motion perception deficit and to compare the developmental trajectories of the two groups on each of the tasks. The main findings were that children with autism were impaired in the perception of biological motion; sensitivity did not improve with development (i.e. their developmental trajectory was flat). This could not be explained by a perceptual impairment as there were subgroups of children on motion tasks with scores in the normal range who were nevertheless performed atypically on the biological motion task. In contrast, the ability to perceive contours from static Gabor signals develops normally in children with autism.
Keywords: autism, biological motion, form-from-motion, motion coherence, developmental disorders, trajectory analyses
Introduction In a recent study Blake et al. (2003) reported that children with autism were less able to perceive biological motion than typically developing children. When shown computer-presented displays of point-light dots moving as if attached to the joints of a human, and scrambled moving dots with the same degree of movement, they were less able to distinguish which displays represented human action and which were scrambled. This result was surprising given how early occurring and robust the perception of biological motion is in typical development. Infants as young as 3 months can distinguish between biological motion point-light displays and scrambled motion point-light displays (Fox & McDaniel, 1982) and typically developing 5 year olds can identify the point-light biological motion of humans and other animals (Pavlova, Krageloh-Mann, Sokolov & Birbaumer, 2001).
If individuals with autism really do have a deficit in the perception of biological motion, it might play a causal role in the atypical development of other cognitive and perceptual systems. Both biological and environmental factors are likely to contribute to the atypical development of autism (Happé, Ronald & Plomin, 2006). An early occurring deficit in orienting to biological motion would be consistent with the view that early deficits contribute to the serious social impairments in autism (Annaz, Milne, Campbell, Coleman & Swettenham, submitted; Dawson et al., 2004). In either case, it is important to know more about the developmental trajectory and the specificity of any deficit in the perception of biological motion.
Is the rate of
development atypical or normal? Do children with autism perform differently at all stages of development? Are there other similar movement perception tasks on which children with autism perform poorly on relative to controls?
In Blake et al’s (2003) study, each child was presented with a 50-trial sequence of 1 second displays of point-light movement, 25 depicting human action and 25 depicting a scrambled display of moving dots. They were asked to identify whether the sequence was a person or not. Signal detection analyses revealed that the group of children with autism was less sensitive in their detection of biological motion than a mental-age-matched group of typically developing children. Two other studies which involved longer presentations and required participants to name biological motion stimuli (Hubert et al., 2007; Moore et al., 1997) have also shown that individuals with autism are impaired relative to controls at naming emotions depicted by point-light movement. However, when asked to name point-light displays depicting simple actions such as kicking and digging, there were no differences between participants with autism and controls. The authors argued that the impairment in biological motion perception is specific to displays depicting emotion. Their evidence suggests that participants with autism can name simple biological motion displays if given enough time, but this does not rule out the possibility that they are less sensitive to biological motion stimuli. Finally, using fMRI Herrington et al. (2007) measured brain activity in individuals with autism spectrum disorder (ASD) while observing biological motion stimuli. The authors reported less activity relative to control participants in inferior, middle and superior temporal regions, including V5/MT. It remains unclear from these data, however, whether all children with autism are less sensitive to biological motion or just a subgroup of this population, or whether the perceptual ability is delayed or developing atypically.
There is also evidence that children with autism are impaired on other motion perception tasks. A number of studies have reported that there are at least some
individuals with autism who are less sensitive to global motion stimuli (Bertone, Mottrom, Jelenic & Faubert, 2003; Milne et al., 2002; Pellicano, Gibson, Mayberry, Durking & Badcock, 2005; Spencer & O’Brien, 2006; Spencer et al., 2000; see also Milne, Swettenham & Campbell, 2005 for a review) have reported data showing that a group with autism was impaired relative to a control group in the perception of second order (texture defined) motion stimuli. The existence of deficits in more than one type of motion task has led to the suggestion that there may be a single underlying cause accounting for a motion perception deficit. For example, a number of authors have argued that a general vulnerability of the dorsal stream underlies atypical performance on motion perception tasks (Spencer et al., 2000; Milne et al., 2002; Blake et al 2003), whilst Bertone and colleagues (2005) have suggested that a general abnormality in neurointegrative mechanisms in the visual cortex results in a deficit in feature integration of complex stimuli (i.e. stimuli which require processing beyond the level of V1; see also Grice et al., 2001) which would include biological motion, global motion and texture defined motion. However, before speculating about a common cause we need to know whether individual children with autism do in fact show deficits across different motion perception tasks.
One way forward, then, would be to test a group of children with autism on a wide range of motion perception tasks. This will tell us how universal the motion perception impairment is in the disorder. We can also then examine whether individual children are selectively impaired on specific motion tasks. If so, this might present a problem for the complexity hypothesis (Bertone et al., 2005), since all the motion tasks involve complex feature integration. Recent findings examining perceptual abilities on a range of motion tasks in children with Williams Syndrome
have revealed that they are impaired in their ability to perceive form-from-motion but not biological motion (Reiss, Hoffman & Landau, 2005). The authors propose that the relatively normal development of biological motion perception in Williams Syndrome could be explained by their tendency to be highly interested in social stimuli. There has not yet been an investigation of different aspects of motion perception in the same cohort of individuals with autism, nor have individual data been presented, something which would shed light on whether there are a range of motion impairments in the same individuals and whether this stems from a common route.
In the current experiments, we tested a group of children with autism on several different motion perception tasks and on a contour integration task using Gabor signals stimuli (Kovacs, Polat, Norcia, Pennefather & Chandna, 2000). In the first experiment we attempted to replicate Blake et al.’s (2003) finding by presenting children with brief displays of point-light biological motion and point-light scrambled motion, measuring their ability to discriminate using signal detection analysis. In the second experiment we used a procedure similar to Jordan, Reiss, Hoffman and Landau (2002), Reiss et al. (2005) and Friere, Lewis, Maurer and Blake (2006) embedding motion stimuli in noise and gradually increasing the noise to signal ratio using a staircase procedure to establish a threshold at which the stimuli could be reliably perceived. One advantage of this procedure when using point-light displays, for example, is that increasing the noise (point-light dots moving in and around the biological motion display) limits the ability to discriminate biological motion from just one or two correspondences of dots (e.g., foot and knee) as the number of potential, but incorrect, correspondences increases with increasing noise. It is then hard to perceive biological motion from just part of the display. In this experiment we
therefore examined thresholds for perception of 1) biological motion, 2) coherent motion, and 3) form-from-motion.
In the biological motion task, participants were asked to discriminate between a pointlight walker and a scrambled walker. In the coherent motion task, the participants were asked to identify the direction of flow (left or right) produced by the percept of motion from a percentage of moving dots apparently moving together one way. In the form-from-motion task, coherent motion within a rectangle revealed the orientation of the rectangle (upright or sideways). In our final experiment, we examined performance on a contour integration task using Gabor signals. Gabor signals model the receptive field of simple cells in area V1, and their integration in the perception of a contour such as a circle cannot be done using global cues such as orientation, colour or texture. Global patterns only emerge through local integration in V1 (Kovacs, Kozma, Feher & Benedek, 1999). This task therefore represents integration of simple stimuli which we predict to be unimpaired in autism (Bertone et al., 2003; Kemner et al., 2007).
Methodological considerations The use of cross sectional developmental trajectories The majority of studies examining perceptual abilities in children with autism have used cross sectional designs, matching children from the disorder group with typically developing control group based on chronological age or mental age. If the group of children with autism perform significantly worse than the control group, they are often described as impaired (and we have used this terminology so far in the current introduction). One problem with such designs is that they give little sense of how task
performance develops with age, something which we would argue is particularly important when studying a developmental disorder such as autism. Although one would ideally use a longitudinal design to study development, cross-sectional studies can give an initial approximation of respective developmental trajectories (Thomas, Annaz, Scerif, Ansari, Jarrold & Karmiloff-Smith, 2008), and these can then be validated by a longitudinal follow-up. The cross-sectional method we used begins by constructing a typically developing trajectory for each task. The trajectory of the autism group is then compared to this reference in a number of ways. A trajectory that links changes in performance to chronological age establishes whether the autism group shows any behavioural deficit on the task. Trajectories linking performance to measures of mental age indicate whether the behavioural deficit is in line with the developmental state of other aspects of the cognitive system. If there is no reliable relationship between age and performance in the children with autism, and a trajectory cannot be constructed, this may still be informative as we can examine whether this is indicative of a flat or zero trajectory or of individual differences, independent of age, within the group. In order to use this design, it is important that the tasks used are sensitive to developmental change. The tasks we have chosen are ideally suited to this design as there is existing evidence that normally developing children continue to improve in performance on different types of motion perception from early to middle childhood (Coch, Skenzel, Grossi & Neville, 2005; Friere et al., 2006; Gunn et al., 2002). In the current study we used this method to assess the development of motion perception in children with autism aged 5 to 12 years.
Method Participants Twenty three children with autism (age range 5:0-12:2 years old, M = 8:10) and 34 typically developing children (age range 4:6-12:3 years old, M = 8:3) participated in the current study. All of the children in the group with autism met established criteria for autism, such as those specified in DSM-IV (American Psychiatric Association, 2000) and had previously received a diagnosis for autism by trained clinicians. None of the children with autism had received any other diagnosis. All participants had normal or corrected-to-normal vision. The experimental protocol was approved by the Ethics Committee, University College London, and both parental informed consent and the child’s assent were obtained before participation. Children from both groups were assessed on a number of standardised tests including the British Picture Vocabulary Scale II (Dunn, Dunn, Whetton & Burley, 1997) and Pattern Construction subtest from the British Ability Scale II (Elliott, Smith & McCulloch 1997). Children in the autism group were also assessed on Childhood Autism Rating Scale (CARS) (Schopler, Reichler & Renner, 1986). See Table 1 for details.
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Apparatus The current study was conducted using stimuli presented on a HP laptop running custom software written with Microsoft Visual Basic and presented on a 15-inch flatpanel LCD screen (1024 x 768 pixel resolution; 60 Hz frame rate). Viewing distance was approximately 40cm.
Experiment 1: Perception of Biological Motion (normal vs. scrambled) Stimuli Point-light displays (Johansson, 1973) were created using a Markerless motioncapture method and were composed of 13 signal dots attached to the joints of an invisible human figure (head, 2 shoulders, 2 elbows, 2 hands, 2 hips, 2 knees and 2 feet). The figure was presented from a side-view (approximately 7.8° visual angle in height) and remained in the centre of the panel as if walking on the spot. Further four figures were created (running, throwing, kicking and star-jumping) resulting in a set of five “in-phase” person-like animations (see Figure 1A). Corresponding out-ofphase “scrambled” stimuli were created for each of the five actions by taking each trajectory of each dot and playing them temporally out of phase with each other (hence controlling for display density and overall movement). Each animation was presented as white dots on a black panel (17.1° x 17.1° visual angle). The duration of each trial was 1 second, followed by inter-stimuli fixation cross.
Procedure The task began with 10 practice trials (5 point-light walkers - PLW and 5 scrambled PLW trials, presented randomly), the first 5 trials were presented on the screen until a response was made and the second 5 trials were presented for 1 second duration. In the practice session, each child was told that during the game he/she would sometimes see dots that “moved like a person” and sometimes dots that would “moved in a funny way and not really like a person”. The keyboard of the computer was covered with black card such that only two keys were visible: z and m. These keys were covered by Y and N stickers respectively. Participants were told to press “Y” if the dots were moving like a person and to press “N” if they were not. Once the child was familiar
with the procedure, the 40 experimental trials (each with a duration of 1 second) were then presented in random order with constraints such that no more than two of the same action or same phase could appear consecutively. The experimenter controlled the progression of the task by clicking a button to initiate each subsequent trial
Experiment 2: Sensitivity to Motion Tasks These tasks examined whether children with autism have altered sensitivity to detect different types of motion. Three tasks were developed based on a procedure used by Reiss et al. (2005): biological motion, form-from-motion and motion coherence.
Stimuli Biological Motion Task This task was designed to establish thresholds for the detection of a point-light walker in noise. In this task, in-phase and scrambled point-light walkers (as shown in Figure 1B) were presented side by side. During each trial, PLW (in-phase and scrambled) were fixed in the display’s centre while walking on the spot towards either left or right. The first trial contained only signal elements (PLW alone), and groups of three distractor dots were added or removed on subsequent trials depending on accuracy of response. Participants were asked to press a button which corresponded to a panel where they could see “dots that look like a person walking”. Following two consecutive correct responses 3 noise elements (distractor dots) were added to the display. An incorrect response caused six noise elements to be removed.
Motion Coherence Task This task was designed to establish motion coherence thresholds for each respondent. Two black panels were displayed on the screen, each containing ten randomly positioned signal elements. In one of the panels, signal elements moved all together in the same direction (3.21°/s) while, in the other panel, signal elements moved randomly to new locations within the panel. Each signal element had a lifespan of one frame (limited lifetime technique: Newsome & Pare, 1988) in order to ensure that one particular element could not be followed through a trial. Participants were asked to detect which set of dots were moving in the same way “like swimming fish”. Two consecutive correct responses led to the addition of 3 noise elements to both panels and an incorrect response led to the removal of 6 noise elements.
Form-from-Motion Task This task was designed to establish form-from-motion thresholds for each respondent. In each of two black panels signal elements were arranged into a rectangular figure and surrounded by background noise elements. The figure and background elements moved coherently in opposite directions (3.21°/s) and noise elements (with random motion) were present in both the figure and the background. In one panel the figure was horizontal and in the other the figure was vertical. The task involved identifying the panel containing the vertical rectangle. Participants were told that there was a rectangle hidden inside each panel on the screen. A cardboard rectangle of similar size and shape was presented to the child to ensure that they understood what shape they were looking for. The cardboard shape was then rotated to a vertical position and the participant was directed to look for the “rectangle that is standing up on its end” and to press the button underneath that panel. The overall density of dots was constant
throughout the task and difficulty was manipulated by converting signal elements to noise elements. Two consecutive correct responses led to the conversion of 3 signal elements into noise elements and an incorrect answer changed 6 noise elements back to signal elements.
General Procedure Participants completed all motion tasks in separate blocks presented in counterbalanced order. Each child was tested separately in a quiet room. For each task, participants were asked to indicate which panel contained the target stimuli, by pressing a button underneath the relevant panel. Perceptual thresholds were established using a 2-down/1-up adaptive staircase rule on each of the motion tasks. Three noise dots were added to the target and adjacent distractor panel after every two consecutive successful trials. However, if the child responded incorrectly on a trial then six noise dots were subtracted, making it easier to perceive the target. The task continued until 7 reversals had taken place (i.e. 7 correct followed by incorrect trials). The average signal to noise ratio (signal elements divided by signal + noise) of the 7 reversals was calculated to establish the threshold.
Experiment 3: Static Contour Integration Task Stimuli Sensitivity for integration of local elements to a global pattern was measured by the use of a closed chain of colinearly aligned Gabor signals (contour) and a background of randomly oriented and positioned Gabor signals (noise) (created by Kovacs & Julesz, 1993). Spacing between elements along the contour and spacing in the background were controlled independently. At small signal-to-noise ratios,
background elements were allowed to get into the spaces between contour elements, but orientational alignment was avoided. A different random shape and background were computed for each card. The difficulty level of each card was determined by the relative density of noise elements and expressed as a ratio of average noise spacing over contour spacing (D). Absolute contour spacing is expressed in Gabor wavelength units (l). The strength of spatial interactions subserving contour integration in an individual is indicated by the value of D at their threshold. An example of the contour-integration stimuli is shown in Figure 6 (see Kovacs et al., 1999; Kovacs et al., 2000 for details).
Procedure Initially, each participant was asked to draw a circle to ascertain that he/she could recognize a circle when asked. If this was done correctly, the participant was presented with one of the two sets of cards presented at approximately 40 cm distance. The participant’s task was to identify the location of the contour by tracing its path with their finger. Each child was presented with one practice trial to ensure that he/she understands procedure of the task. The cards were presented in an increasing order of difficulty and children were given a 6 seconds limit to given an answer. The last correctly identified target was recorded as a threshold (D). D is varied between 0.5 and 1.2 in steps of 0.05, resulting in 15 cards in the set. A simple staircase procedure was used in which threshold was identified by the last correctly identified card.
Results The data were analysed as follows: (i) We first examined developmental trajectories for each group for each task. Each developmental trajectory was modeled by a linear function relating individuals’ d-prime (d’) scores (Experiment 1) or thresholds (Experiments 2 and 3) to chronological age; (ii) if both groups showed a reliable linear relationship between the dependent variable and age, this was followed by a direct comparison between the groups (using cross sectional ANCOVA) to determine whether the performance of the children with autism differs in terms of onset and rate of development; (iii) finally, performance values were plotted against mental ages from the British Picture Vocabulary Scale II (BPVS) and Pattern Construction subtest from the British Ability Scale II (PC) tasks to explore whether performance is in line with a given standardised measure (see Thomas et al., 2008, for a similar approach). D’ values were used in Experiment 1 because they take into account hits (respond “person” to a PLW trial) and false alarms (respond “person” to a scrambled PLW trial) and therefore measure perceptual sensitivity independent of bias on force choice paradigms (Macmillan & Creelman, 1991). D’ value of 0 indicates that participants are at chance level on the task.
Experiment 1: Perception of Biological Motion (normal vs. scrambled) D’ values were calculated for each individual child. The average d’ values for the TD children and for children with autism were 2.2 and 1.0 respectively. Figure 2 shows d’ value for each individual and trajectory each group. Initial linear regressions revealed that d’ values increased reliably with chronological age in the TD children [R2 = .48, F(1,33) = 29.25, p
