Post on 11-Feb-2020
Motion perception and autistic spectrum disorder
1
Motion perception and autistic spectrum disorder: A review.
Elizabeth Milne CA
Department of Psychology, University of Sheffield
Western Bank, SHEFFIELD, S10 2TP, UK.
+44 (0) 114 2226558, Fax: + 44 (0) 114 2766515
E.Milne@Sheffield.ac.uk
John Swettenham & Ruth Campbell
Department of Human Communication Science, University College London
Chandler House, 2 Wakefield Street, LONDON, WC1N 1PF, UK.
J.Swettenham@ucl.ac.uk R.Campbell@ucl.ac.uk
This is a reprint of an article printed in the February – April issue (2005) of Cahiers
de Psychologie Cognitive / Current Psychology of Cognition, volume 23 (1 – 2), pp 3
– 33.
Motion perception and autistic spectrum disorder
2
Abstract
Recent evidence has indicated that some children with autistic spectrum disorder
(ASD) show reduced ability to detect visual motion. The data suggest that this
impairment is present in children with a range of autistic spectrum diagnoses, but not
present in all children diagnosed with ASD. The occurrence of abnormal motion
perception in children with ASD has led to speculation regarding the root of this
impairment. Hypotheses regarding reduced sensitivity of the visual magnocellular
system / cortical dorsal stream (Milne et al., 2002; Spencer et al., 2000) and reduced
neuronal integration (Bertone et al., 2003), will be discussed in this review. Clinical
implications of the impairment, such as the degree to which motion perception may be
related to diagnostic criteria and /or symptom severity in ASD, and the relationship
between abnormal motion perception in autistic spectrum, and other, non-autistic
spectrum developmental disorders will also be discussed. The conclusion is drawn
that more research should be carried out including larger samples of participants, and
that in future studies researchers should provide details of the variability of
performance in their data, and investigate relationships between motion perception,
diagnostic criteria, symptom severity and other potential correlates which, it is hoped
will lead to further understanding of the implications of abnormal motion perception
in ASD.
Key words
Autistic spectrum disorder, motion perception, visual system, developmental
disorders.
Motion perception and autistic spectrum disorder
3
Autistic spectrum disorder (ASD) is a family of pervasive developmental
disorders, usually diagnosed in childhood. Within the autistic spectrum are autistic
disorder, diagnosed on the basis of impairments in social interaction, communication,
and repetitive, stereotyped patterns of behaviour (American Psychiatric Association,
1994); Asperger’s disorder, which is popularly characterised as a less severe form of
autistic disorder but in actuality is diagnosed on the basis of impairment of social
interaction, accompanied by repetitive, stereotyped behaviour, but without a
significant impairment in communication (American Psychiatric Association, 1994);
and pervasive developmental disorder not otherwise specified (PPD-NOS), which is
diagnosed on the basis of impairment in social interaction or communication skills, or
when stereotyped behaviours are present, but the full criteria for a specific pervasive
developmental disorder are not met. This category includes atypical autism which is
diagnosed when presentations do not meet the criteria for autistic disorder because of
late age of onset, atypical symptomatology, subthreshold symptomatology, or all of
these (American Psychiatric Association, 1994). ASD affects over 500,000 families
in the UK (National Autistic Society, 2004). A recent meta-analysis of 19 international
epidemiological surveys carried out since 1987 has indicated that the prevalence of
autistic disorder is 10 cases in every 10,000 (Fombonne, 2003). In the same study, the
prevalence of Asperger’s disorder and PDDNOS was estimated to be 2.5/10,000 and
15/10,000 respectively, giving a current estimate of the occurrence of ASD as
27.5/10,000. The origins of ASD are currently unknown, although evidence points to
a genetic link, which at some time during early development impacts on subsequent
brain development (for a review of genetic research on ASD see Muhle, Trentacoste,
& Rapin, 2004). In addition to the impairments of social interaction, communication
and repetitive behaviour, other symptoms are often present, such as abnormal
responses to sensory stimuli, hyper-sensitivity to sound or touch, and disturbances in
visual perception (Talay-Ongan & Wood, 2000; O'Neill & Jones, 1997; Rogers,
Hepburn, & Wehner, 2003). In particular, recent research suggests that the ability to
detect moving stimuli is abnormal in some individuals with ASD (Bertone, Mottron,
Jelenic, & Faubert, 2003; Blake, Turner, Smoski, Pozdol, & Stone, 2003; Gepner &
Mestre, 2002; Gepner, Mestre, Masson, & De-Schonen, 1995; Milne et al., 2002;
Milne et al., in press; Spencer et al., 2000). The aim of this paper is to review the
literature which has investigated motion perception in individuals with ASD and to
Motion perception and autistic spectrum disorder
4
discuss the implications arising from this research. The implications will be
considered from two angles;
1) What, if anything, can a motion perception impairment in ASD currently tell
us about the neuronal architecture of ASD?
2) What are the clinical implications of a motion perception impairment in ASD?
For example, how might motion perception impairment impact on other
perceptual / cognitive abilities? And what is the relationship between
abnormal motion perception in ASD and the impaired ability to detect
coherent motion which has been reported in other non autism spectrum
developmental disorders?
Finally, a summary of outstanding questions will be presented, and new areas of
research will be highlighted which may lead to further understanding of the neural
correlates of autistic spectrum and other developmental disorders.
Evidence of abnormal motion perception in individuals with ASD
Postural stability in response to optic flow
The first published study which suggested that children with autistic disorder
may perceive motion in a different way to typically developing children reported that
when standing on a force platform and presented with optic flow, children with
autistic disorder were less posturally reactive to visual motion than typically
developing controls (Gepner et al., 1995). The results of this study were extended in
2002, by additional data which demonstrated that in a different sample of participants,
three children with autistic disorder and developmental delay (mean age of 9 years, 5
months) showed less postural reactivity to visual motion than both a typically
developing control group (mean age 8 years, 2 months) and a group of three children
with Asperger’s syndrome and normal IQ (mean age 7 years and 5 months), who in
fact showed increased postural activity compared to the control group (Gepner &
Mestre, 2002). It remains to be seen whether postural hypo-reactivity in children with
autistic disorder arises as a result of reduced sensitivity to dynamic stimuli, abnormal
postural control, or both.
Sensitivity to coherent motion
Coherent motion is a global motion signal that is apparent from the integration
of locally moving elements. Sensitivity to coherent motion can be measured by
Motion perception and autistic spectrum disorder
5
manipulating the number of coherently moving local signals within an array of
dynamic noise presented in a random dot kinematogram, as shown in figure 1.
A high proportion of coherent elements renders global coherent motion easier to
detect than a lower proportion. Coherent motion sensitivity can thus be determined by
a threshold for detection of coherent motion, a low threshold (low proportion of
coherently moving dots needed to detect coherent motion) reflects good sensitivity
whereas a high threshold (high proportion of moving dots needed to detect coherent
motion) reflects poor sensitivity.
Insert figure 1 about here please
Two research groups have reported significantly increased motion coherence
thresholds in children with autistic disorder as compared to controls (Milne et al.,
2002; Spencer et al., 2000), suggesting reduced sensitivity to coherent motion in
children with autistic disorder. Spencer et al. (2002) found elevated motion coherence
thresholds in children with autistic disorder (verbal age range from 7 -11 years)
compared with those of verbal-age matched typically developing children, whereas
Milne et al. (2002) found elevated thresholds in children with autistic disorder and
normal intelligence (mean age 11 years, 8 months) as compared to typically
developing children matched for chronological age and non-verbal ability (mean age
11 years and 7 months). Spencer et al. (2000) further demonstrated that the
participants with autistic disorder in their sample were not impaired at detecting
coherent form in a control task (see figure 2) which was similar in application to the
coherent motion detection task but which recruited a visual sub-system that is unlikely
to be involved in the detection of coherent motion. That is, reduced sensitivity to
coherent motion in children with autistic disorder did not occur as a result of a general
visual impairment or other task factors such as a lack of task attention or motivation.
Additionally, because the form control task also involves integrating local elements
(static lines) into a global percept (of a circle), it is unlikely that the high motion
coherence thresholds shown by the individuals with autistic disorder were due to a
failure to integrate local elements into a global percept, as may be suggested by a
model which attempts to explain the data in terms of the reduced integration of
perceptual information, or “weak central coherence” (cf Frith, 2003).
Motion perception and autistic spectrum disorder
6
Insert figure 2 about here please
Sensitivity to biological motion
Biological motion is the term used to characterise any perceived animate
movement, such as gait (posture and movements of walking), sitting, cycling,
jumping etc. The human visual system is extremely sensitive to biological motion.
This is shown by the fact that even when visual information is reduced to a point-light
display, tracking movement at the joints of limbs (see figure 3), people can reliably
identify and discriminate complex stimulus sequences (Johansson, 1973), as well as
subtle social information such as the gender and emotional state of the actor (Cutting
& Kozlowski, 1977).
Insert figure three about here please
Infants of 3 months can distinguish between biological and non-biological
motion portrayed in point-light displays (Fox & McDaniel, 1982), and children as
young as 3 years can reliably recognise different types of biological motion, such as
human and non human (animal) forms (Pavlova, Krageloh-Mann, Sokolov, &
Birbaumer, 2001). To date, there have been two published studies investigating the
perception of biological motion in autistic disorder (Blake et al., 2003; Moore,
Hobson, & Lee, 1997). Moore et al. (1997) presented children with autistic disorder
and below average ability (as measured by the British Picture Vocabulary Scale, mean
chronological age of the sample 14 years, 10 months) and non-autistic learning
disabled children (mean chronological age 14 years, 2 months) with brief video
sequences of point-light displays depicting a human actor walking across the screen,
or the movement of an object such as a chair being rotated or a ball bouncing. The
participants were asked to identify the stimulus by answering the question “What are
the dots stuck to?” The dependent variable reported was the length of time needed to
view the stimulus before correctly identifying the person depicted in the point light
display. The results indicated that while there was a trend towards poorer
performance among children with autistic disorder compared to the non-autistic
controls when the images were presented at short (<1000 msec) exposure duration
and with only 5 point lights in the display, overall the children with autistic disorder
were not impaired at detecting the person from the array of moving point-lights.
Motion perception and autistic spectrum disorder
7
Additionally with a 10 light display, both the children with and without autistic
disorder recognised the person at a similar time duration to that of normal adults –
approximately 200 msec (Johansson, 1973). However, Blake et al. (2003) have
reported that children with autistic disorder are less able than typically developing
children to detect biological motion from point light displays. Blake et al. also tested
children with autistic disorder and developmental delay (aged between 8 and 10
years) – and a group of typically developing children who were chronologically
younger (aged between 5 and 10 years), but matched in terms of mental age. This
study differed from Moore et al.’s study as the participants were not required to
identify the object depicted in point lights, but to simply detect whether a point-light
stimulus showed a person or not (i.e. a two alternative forced-choice). 50% of the
stimuli depicted a human actor engaged in activity such as running, kicking, climbing,
throwing or jumping, whereas the remaining half of the stimuli were phase-scrambled
sequences containing the same amount of absolute motion as the target stimuli but
without producing a recognisable percept. Under these conditions children with
autistic disorder had significantly lower d’ scores than the typically developing group,
indicating reduced sensitivity to biological motion in the children with autistic
disorder. Again, in line with Spencer et al. (2000), despite having reduced sensitivity
to biological motion, the children with autistic disorder showed no differences
compared to controls in their ability to accurately detect coherent form in a control
task. One caveat about this study should be noted however; the children with autistic
disorder in the sample were developmentally delayed and were matched to a group of
typically developing younger children. Therefore it could be possible that the children
with autistic disorder showed less sensitivity to biological motion because of general
developmental delay rather than being specifically related to autism.
Sensitivity to second order motion
As Mather & Murdoch have described; “First order stimuli contain stable and
coherent spatio-temporal energy corresponding to the velocity of motion. Second-
order stimuli do not contain coherent energy but, instead, motion information is
conveyed by contours with dynamically changing and/or incoherent Fourier energy
(texture borders, for instance)” (Mather & Murdoch, 1997 p 605). Thus, first-order
refers to motion which is perceived on the basis of luminance change over time, and
second-order refers to motion which is perceived on the basis of changes in
Motion perception and autistic spectrum disorder
8
characteristics other than luminance (such as contrast) over time (Clifford & Vaina,
1999). In order to investigate the perception of first- and second- order motion in
autism, Bertone et al. (2003) devised a task in which the perception of motion in
radiating, rotating and translating patterns was mediated by either first- or second-
order motion cues (luminance and contrast respectively). A schematic illustration of
these stimuli is presented in figure 4.
Insert figure 4 about here please
Bertone et al. found that the participants with autistic disorder and normal IQ
(mean chronological age 12.18 years) showed no deficit in their ability to detect the
direction of motion from these patterns when the stimuli were mediated by first order
characteristics (luminance), but when motion was defined by second order
characteristics (contrast), participants with autistic disorder were significantly
impaired compared to a chronological age matched control group (mean
chronological age 13.13 years). Bertone et al. suggested that individuals with autism
do not show abnormal perception of motion per se, but that the reported reduction in
their ability to detect motion could be related to the complexity of the stimulus. They
further suggested that the results of their study may reflect an impairment of
integrating complex stimuli in autism. They point out that to discriminate global
motion patterns, such as coherent motion, the visual system must first integrate local
motion signals, therefore reduced performance on these tasks could be explained by a
deficit of integrating complex information at a perceptual level.
Summary
Considering all the data regarding motion perception in ASD, it appears that
some children with autistic spectrum diagnoses are less able to detect motion stimuli
than matched controls. What, if anything, does this suggest about the neuronal
architecture of ASD? This issue will be considered below. However, in order to
consider the implications of reduced sensitivity to motion in ASD, it is necessary to
briefly review the anatomical architecture which underlies intact motion perception.
The functional anatomy of motion perception in the human visual system.
Motion perception and autistic spectrum disorder
9
The human visual system has been broadly defined as consisting of two
parallel but interconnected streams of cortical areas; the dorsal and the ventral stream
(Ungerleider & Mishkin, 1982). It is thought that motion perception is governed by
structures of the dorsal stream, whereas the ventral stream is specialised for form and
colour perception. Specialisation for motion perception occurs very early in the visual
system, as specific retinal neurons (known as α cells and β cells) channel information
into two parallel pathways; the magnocellular and parvocellular pathways which are
thought to be specialised for motion and form perception respectively. The axons
from retinal α and β cells form separate streams within the optic nerve and innervate
different layers of the lateral geniculate nucleus (LGN). The LGN consists of 6-layers,
layers 1 and 2 receive input from only α ganglion cells and layers 3 – 6 receive input
from the β ganglion cells. Layers 1 and 2 contain large cell bodies, known as
magnocells, whereas layers 3 – 6 contain smaller, parvo, cells. The magnocellular and
parvocellular pathways are separated not only anatomically, but also functionally.
Magnocellular neurons respond preferentially to low-spatial and high-temporal
frequency stimuli, e.g. motion and flicker, whereas parvocellular neurons respond
preferentially to high-spatial and low-temporal frequency stimuli, e.g. static stimuli
(Derrington & Lennie, 1984). Cortical motion perception is therefore thought to be
dominated by inputs from the magnocellular pathway. This has been demonstrated
experimentally by studies which selectively lesion either the magnocellular or
parvocellular layers of the monkey LGN; lesioning the magnocellular layers leaves
the monkey motion blind, whereas lesioning the parvocellular layers leaves motion
perception intact (Schiller, Logothetis, & Charles, 1990).
To some extent the segregation of magnocellular and parvocellular channels is
preserved into the cortex, with axons from the two streams innervating different
layers of cortical area V1 (Nealy & Maunsell, 1994), however, via the blobs and
interblobs of V1 and the thick and thin stripes of V2 (Wong-Riley et al., 1993),
neuronal intermixing occurs, and the ventral stream receives input from both the
magnocellular and parvocellular layers of the LGN, whereas the dorsal stream
receives input mainly from the magnocellular layers (Nealy & Maunsell, 1994). The
ventral stream includes area V1, extra-striate areas V2, V4, and areas of the infero-
temporal cortex, the dorsal stream includes area V1, extra-striate areasV2, V5 (or
medial temporal area MT), and areas of the posterior parietal cortex (Milner &
Goodale, 1995). Functional imaging has shown that several cortical areas, mainly
Motion perception and autistic spectrum disorder
10
defined as forming part of the dorsal stream, are active during the presentation of
moving stimuli. V1 is activated by many classes of moving stimuli, including flicker
and dynamic noise, suggesting that this area responds to general spatiotemporal
luminance modulations (Smith, Greenlee, Singh, Kraemer, & Hennig, 1998). Area
V5, which lies at the juncture of the temporal, parietal and occipital lobes (Sunaert,
Van Hecke, Marchal, & Orban, 1999) is perhaps the most well defined area in terms
of motion perception. Converging data from single cell recording (Britten, Shalden,
Newsome, & Movshon, 1992), lesion studies (Newsome & Pare, 1988, Zihl, Von
Cramon, Mai, & Schmid, 1983) and fMRI (Zeki et al., 1991) all report an essential
role of area V5 in motion perception. Specifically, cells in area V5 are particularly
sensitive to coherent motion. This has been demonstrated by monkey single cell
recording (Britten et al., 1992) and human fMRI, which has also elucidated other
areas, such as area V3, V3a and discrete foci in the intraparietal sulcus which are also
activated by coherent motion (Braddick et al., 2001).
A double dissociation of motion impaired patients suggests that perception of
first- and second- order motion may also be cortically segregated. A patient with a
brain lesion close to the surface of the occipital lobe, probably encompassing areas V2
and V3, has been reported to show a selective impairment of first-order motion
perception (Vaina, Makris, Kennedy, & Cowey, 1998), whereas a patient with a
cortical lesion close to area MT appears to have a selective impairment of second-
order motion perception (Vaina & Cowey, 1996).
Biological motion also appears to activate discrete cortical areas, notably the
superior temporal sulcus (STS), quite distinct from those activated by coherent motion
or specific first or second order motion signals (Battelli, Cavanagh, & Thornton,
2003). Functional imaging has revealed increased activation in the STS region during
perception of hand action, mouth movement, lip-reading, body movement and eye
gaze (Calvert, Campbell, & Brammer, 2000; Puce, Allison, Bentin, Gore, &
McCarthy, 1998.Grezes et al., 2001; Howard et al., 1996, for a review see Puce and
Perrett 2003). Cells in the STS region of the monkey cortex have been found which
are responsive to the sight of a hand purposefully manipulating an object, but are
unresponsive to the sight of tools manipulating the same object (Jellema, Baker,
Wicker, & Perrett, 2000). Similarly, Oram and Perrett have reported cells in the upper
bank of the monkey STS which fire in response to moving hands and faces but not to
movement elicited by inanimate objects (Oram & Perrett, 1994). In humans, areas of
Motion perception and autistic spectrum disorder
11
the STS, particularly the posterior STS (Bonda, Petrides, Ostry, & Evans, 1996;
Grossman et al., 2000) and the superior temporal polysensory area (STP) (Vaina &
Gross, 2004) are particularly sensitive to point-light displays of biological motion,
therefore this area is thought to be important both in the extraction of form from
motion, and may also be implicated in the detection and recognition of the behaviour
of others (Puce & Perrett, 2003). Recent data using the technique of
magnetoencephalography (MEG) suggests changes in neuromagnetic gamma activity
correlate with ability to extract structure from motion, and coincide with task-related
cortical activity as measured by fMRI (Singh, Barnes, Hillebrand, Forde, & Williams,
2002). By measuring oscillatory gamma brain activity using MEG, Pavlova et al. have
demonstrated that the brain can dissociate coherent structure conveyed by biological
motion as early as 100 ms after stimulus onset. By 130 ms, activity over the parietal
lobes indicates that the brain can distinguish between a regular point light walker and
a scrambled one, suggesting that the detection of biological motion is achieved at
relatively early stages of cortical processing (Pavlova, Lutzenberger, Sokolov, &
Birbaumer, 2004).
What is the aetiology of impaired motion perception in ASD?
Findings of reduced sensitivity to motion in individuals with ASD have led to
differing suggestions as to the possible aetiology of this impairment. At present, no
firm conclusions can be drawn. However two main suggestions run through the
literature. Some researchers have suggested that impaired motion perception in ASD
could arise from an abnormality in the particular area of the visual system implicated
in visual motion perception, namely the (sub-cortical) magnocellular system or the
(cortical) dorsal stream (Milne et al., 2002; Spencer et al., 2000). Other researchers
(Bertone et al., 2003), reporting that individuals with ASD have reduced sensitivity to
second- but not first-order motion, have suggested that the structural architecture
which underpins motion perception is intact and that impaired motion perception may
indicate reduced ability to integrate complex perceptual information. However, as yet
there is no direct evidence to support either one of these positions. Structural
abnormalities of dorsal stream structures are not usually identified in MRI studies of
ASD, although until recently, researchers have not directly investigated these cortical
areas as the majority of ASD MRI studies have focussed on the cerebellum and / or
the hippocampus / amygdala / limbic structures (Brambilla et al., 2003). However,
Motion perception and autistic spectrum disorder
12
neuromagnetic data demonstrated that a group of 4 adults with Asperger’s syndrome
and 1 adult with autistic disorder, showed the same degree of oscillatory brain activity
in the primary motor cortex when viewing human action (Avikainen, Kulomäki, &
Hari, 1999). A functional MRI study of different types of motion perception in
individuals with ASD would help to clarify whether abnormalities in specific areas of
the dorsal stream underlie reduced motion perception in ASD. Similarly, the
magnocellular system has not been investigated directly in ASD. Within the literature
it is unclear to what extent high motion coherence thresholds implicate impairments
of the magnocellular system. Some researchers, drawing from psychophsyiological
evidence that lesions of the magnocellular pathway in monkeys impair coherent
motion detection (Schiller et al., 1990) claim that coherent motion detection
represents a reliable, albeit putative, indicator of the magnocellular pathway
(Cornelissen, Hansen, Hutton, Evangelinou, & Stein, 1998; Milne et al., 2002; Talcott
et al., 1998), whereas others, drawing on further psychophsyiological evidence that
direction discrimination can be retained even after magnocellular lesions (Merigan,
Byrne, & Maunsell, 1991), suggest that coherent motion detection is not a reliable
indication of magnocellular integrity (Skottun, 2000). Further psychophysical tests,
which provide a more direct indication of the integrity of the magnocellular /
parvocellular systems need to be carried out to establish whether high motion
coherence thresholds in children with ASD represent magnocellular impairment. For
example, contrast sensitivity of static and flickering gratings of low and high spatial
frequencies can provide a clearer separation of the sensitivity of the magnocellular
and parvocellular systems, and EEG investigation of visual evoked potentials elicited
by moving / static / coloured stimuli (see Neville & Bavelier, 2000, cf Boeschoten,
Kemner, Kenemans, & van Engeland, 2004) can provide direct data on both the
latency and amplitude of brain responses generated by the specific processing
streams. In addition future post-mortem and histological studies which directly
measure magno- and parvo-cell density in the LGN will be essential if this claim is to
be supported.
As described above, Bertone et al. (2003) have shown that participants with
ASD are just as sensitive to simple first order motion stimuli as matched controls, but
significantly less sensitive than controls to second-order motion stimuli. However,
other studies have shown that when a more complex first-order stimulus is presented
(e.g. a random dot kinematogram), participants with ASD are less able to detect
Motion perception and autistic spectrum disorder
13
coherent motion than controls (Milne et al., 2002; Spencer et al., 2000). To examine
this point it is necessary to clarify exactly what is meant by the terms first- and
second- order motion. As we have stated earlier, first-order motion refers to motion
defined by changes in luminance, and second order motion refers to motion defined
by changes other than luminance. Less straightforward however, is the distinction
between first- and second- order motion detectors, and it remains to be seen whether
the visual system employs separate, independent populations of neurons for the
perception of first- and second- order motion, or whether a single system resolves
both classes of motion. To clearly understand the implications of sensitivity to first-
and second- order motion in individuals with ASD, it is important to bear in mind the
distinction between the physical properties of first- and second- order motion stimuli,
and the psychophysical properties of the motion detectors (see Mather & Murdoch,
1997). The perception of coherent motion from a random dot kinematogram of the
type used by Milne et al., 2002 and Spencer et al., 2000 investigates the global
processing of first order motion. In order to detect coherent motion within this
stimulus participants must integrate the local, first order signals to derive a global
directional signal, i.e. the stimulus is a first-order stimulus (motion within the
stimulus is generated purely by changes of luminance over time), but the operation of
perceiving coherent motion requires additional processing of these first order signals.
This explanation illustrates that the question of abnormal motion perception in
individuals with ASD cannot be reduced simply to a division between the physical
characteristics of first and second order motion stimuli, but that, as Bertone et al.
(2003) suggested, abnormality may occur at the stage at which local motion signals
are integrated. However, contrary to Bertone et al.’s suggestion that impaired
detection of complex motion in ASD can be explained by a “decreased capacity to
integrate complex perceptual information rather than a specific inability to efficiently
process motion information as such” (Bertone et al., 2003 pg 4), the finding that
individuals with autistic disorder who are impaired at detecting coherent and
biological motion show no equivalent impairment in detecting coherent form (Blake
et al., 2003; Spencer et al., 2000) suggests that impairments in the ability to integrate
perceptual information occur in the perception of motion, but not in integrating all
perceptual information.
Clearly individuals with ASD are not motion blind, neither their behaviour not
any test suggests this, what is apparent in the data however is that individuals with
Motion perception and autistic spectrum disorder
14
ASD (or at least, some individuals with ASD as will be discussed below) have
reduced sensitivity to visual motion. Using random dot kinematograms establishes a
threshold for coherent motion detection; every participant is tested until they reach the
level at which they can no longer detect the coherent signal, that is, they are tested to
the limits of their perception. Results arising from these studies show, not that the
participants with ASD cannot perceive motion (either in the noise dots or even the
coherent motion signal), but that some participants with ASD require a denser
coherent signal in order to be able to detect coherent motion. This becomes apparent
only by presenting trials until each participant can no longer perceive the coherent
signal. Similarly, in Bertone et al.’s (2003) data, both the participants with ASD and
the controls were much more sensitive to first- than second-order motion (with log
motion sensitivity dropping from approximately 2.5 in both groups for first order
motion to less than 1 in both groups for second-order motion), indicating that
detection of second order motion in this paradigm is a more difficult task. Task
difficulty could therefore predict whether or not individuals with ASD have impaired
motion perception compared with controls, with only relatively complex tasks being
sensitive enough to measure such an impairment.
When searching for a cause of impaired motion perception in ASD, it is
important to note that reduced sensitivity to certain types of motion stimuli does not
necessarily predict reduced sensitivity to other types of motion stimuli. There may be
systems specialised for perceiving different motion stimuli. For example, case studies
in the literature discuss brain-damaged patients who are impaired at detecting
coherent motion but show no deficit in detecting biological motion (Vaina, LeMay,
Bienfang, Choi, & Nakayama, 1990), and conversely, from patients who are impaired
at detecting biological motion but have no deficit in detecting coherent motion
(Schenk & Zihl, 1997). In addition, as highlighted above, different cortical areas
appear, from fMRI data, to be specialised for the perception of different motion
classes, suggesting that motion perception is not a unitary phenomenon. However, it
is worth noting that whilst there is strong evidence for a dissociation between
performance on motion coherence perception tasks and biological motion perception
tasks in normal (Grossman & Blake, 1999) and brain damaged adults (Battelli et al.,
2003; Viana, Lemay, Bienfang, Choi, & Nakayama, 1990), this does not necessarily
imply that there is no developmental relationship between the two (Bishop, 1997;
Karmiloff-Smith, 1998). Data from adult neuropsychological studies don’t take into
Motion perception and autistic spectrum disorder
15
account the notion that perceptual ability can develop with experience, which could
be akin to specialisation of that ability. It appears that learning, and environmental
factors may affect the developmental trajectory of motion perception. For example,
participants can be trained to discriminate biological motion embedded in dense noise
dots from scrambled motion as (Grossman, Blake, & Kim, 2004), and both
behavioural and neurophysiological studies indicate that sensitivity to visual
movement in the peripheral visual field is greater in deaf than in hearing people, and
may be modified by early exposure to a signed language (Bavelier et al., 2001;
Neville & Lawson, 1987). It has also been shown that individuals with autistic
disorder and learning difficulties can improve their ability to recognise form-from-
motion with training (Carlin, Hobbs, Bud, & Soraci, 1999). It would be interesting to
know whether the visual environment experienced by children with autism influences
the development of motion perception.
Theoretical implications of impaired motion perception in ASD.
Each of the theories highlighted above could lead to further testable
hypotheses about visual perception in ASD. For example it has been hypothesised that
if an impairment of the magnocellular system gives rise to reduced motion perception
in autism, then other perceptual functions which are heavily supported by this system
may also be abnormal in ASD (Milne, 2004). As reviewed above, the magnocellular
system is functionally specialised for the perception of moving and flickering stimuli,
and is thought to transmit lower spatial frequencies to the cortex than the
parvocellular system (Livingstone & Hubel, 1988). A recent report has indicated that
children with autism rely more on high spatial frequency cues when processing faces,
in contrast to typically developing children who rely more on low spatial frequency
cues (Deruelle, Rondan, Gepner, & Tardif, 2004). This finding supports the
suggestion that low spatial frequency information processing may be abnormal in
individuals with ASD. Additionally, recent work has investigated visual evoked
potentials in response to high and low spatial frequency gratings in autism. The results
suggest that both high and low spatial frequencies are analysed differently in children
with autism than controls (Boeschoten et al., 2004). It has been suggested in the
psychophysical literature that low spatial frequencies mediate the perceptual global
bias which is seen in hierarchical stimuli such as Navon-type figures (Badcock,
Whitworth, Badcock, & Lovegrove, 1990; Hughes, Nozawa, & Kitterle, 1996;
Motion perception and autistic spectrum disorder
16
LaGasse, 1993 cf Navon, 1977). Children with ASD have been reported to show
abnormal perception of hierarchical figures (Mottron & Belleville, 1993; Plaisted,
Swettenham, & Rees, 1999; Rinehart, Bradshaw, Moss, Brereton, & Tonge, 2000),
and the degree of global or local bias exhibited in this task is related to motion
coherent threshold such that those children with a local bias had high motion
coherence thresholds (reduced motion sensitivity), whereas those with a global bias
had normal motion coherence thresholds (Milne, Swettenham, Campbell, & Coleman,
2004). This suggests that, if coherent motion detection acts as a reliable indicator of
magnocellular integrity, which, as has been discussed above, it still open for
discussion, then abnormal magnocellular processing may impact on the so-called
unusual cognitive style of reduced global bias / enhanced local bias (cf Mottron,
Burack, Iarocci, Belleville, & Enns, 2003; O'Riordan & Plaisted, 2001) which has
been reported in ASD.
Clearly the implications of impaired motion perception are only just beginning
to be discussed, and the above summary represents a tentative hypothesis. However, it
is presented as an example of new hypotheses which may help to explain cognitive
phenomena of autism based in low-level perceptual aspects of the disorder as opposed
to less clearly defined higher-level models.
Clinical implications of motion perception impairment in ASD.
In addition to investigating what abnormal motion perception may suggest
about the neuronal architecture of ASD, it is important to consider the clinical
implications of abnormal motion perception in ASD. For example, it is important to
ascertain whether abnormal motion perception occurs in all diagnoses within the
autism spectrum. As can be seen from the review of the literature above, the majority
of studies which have investigated motion perception in ASD have recruited children
who have been diagnosed with autistic disorder and who have varying degrees of
developmental delay. Few studies have investigated motion perception in children
diagnosed with other disorders on the autistic spectrum. An exception is Gepner et al.
(2002) who reported that children diagnosed with autistic disorder showed postural
hypo-responsivity in response to visual motion, whereas children diagnosed with
Asperger’s syndrome showed visual hyper-responsivity. This suggests that the exact
nature of autistic spectrum disorder may predict sensitivity to visual motion. However
a recent account of coherent motion detection in children diagnosed with disorders
Motion perception and autistic spectrum disorder
17
that encompass the range of ASDs, has found increased motion thresholds in children
diagnosed with autistic disorder, Asperger’s syndrome and PDDNOS (Milne et al. in
press), suggesting, contrary to Gepner et al (2002) that abnormalities in motion
perception do not occur only in autistic disorder. Blake et al. (2003) reported a
significant relationship between sensitivity to biological motion and severity of autism
as measured by the Autism Diagnostic Observation Schedule, (ADOS, Lord et al.,
2000) and the Childhood Autism Rating Scale, (CARS, Schopler, Reichler, &
Renner, 1988). However, the total number of children in this sample was only 12,
which is a small number for drawing conclusions from correlation data.
It has been reported that individuals with non-specific mental retardation show
impairments in the perception of some types of biological motion (depictions of
throwing rather than depictions of walking) (Sparrow, Shinkfield, Day, & Zerman,
1999), and in the detection of motion defined form (Fox & Oross, 1990). It could be
suggested therefore that learning difficulties associated with ASD may contribute to
poor performance on motion perception tasks. The data appear to contradict this claim
however, as high functioning participants with ASD and without developmental delay
have been reported to show motion impairments when compared to matched controls
(Milne et al. 2002, Bertone et al. 2003). In addition, Milne et al. (in press) did not find
a relationship between coherent motion detection and non-verbal IQ in individuals
with ASD.
Does abnormal motion perception have a causal role in autistic spectrum
disorder? This seems unlikely as not all participants with ASD have impairments in
detecting motion. Milne et al., (2002) highlighted the fact that not all children with
autistic spectrum disorder in their sample showed elevated motion coherence
thresholds, despite an overall mean difference between the groups, and a subsequent
study has reported abnormally high thresholds in only 22% of the ASD group (Milne
et al., in press). Again, the children who showed the largest impairment in detecting
coherent motion had diagnoses which spanned the autistic spectrum and were
unremarkable in terms of non-verbal IQ or chronological age, however no information
regarding symptomatology was available for these children. The reason why some
children with ASD and not others, show elevated motion coherence thresholds
compared to typically developing controls remains to be seen, however, it is
interesting to note that elevated motion coherence thresholds have been recorded in
Motion perception and autistic spectrum disorder
18
individuals with other (non-autistic spectrum) developmental disorders. These data
are reviewed below.
Motion perception impairments in other developmental disorders.
Reduced sensitivity to motion stimuli, at least to coherent motion, has been
reported in other developmental disorders, including dyslexia (Hansen, Stein, Orde,
Winter, & Talcott, 2001; Talcott et al., 1998), William’s syndrome (Atkinson et al.,
1997), and Fragile X syndrome (Kogan et al., 2004). The genetic bases of dyslexia are
still contentious, but both Williams’ and Fragile X syndromes are known to arise as a
result of either a genetic deletion or mutation. Williams’ syndrome results from a
deletion on chromosome 7q11.23, and is characterised by moderate mental retardation
and impaired spatial cognition. Fragile X syndrome arises from a mutation of the
FMR1 gene, leading to a lack of fragile X mental retardation protein (FMRP), and is
characterised by intellectual disability, attention deficit disorders, autistic behaviours
(such as hand-flapping, poor eye contact) and an aversion to touch and noise. Despite
the diverse range of symptoms across the four developmental disorders (ASD,
dyslexia, William’s syndrome and Fragile X syndrome), it is interesting to note that
reduced sensitivity to coherent motion has been documented in all of them. Given that
reduced sensitivity to coherent motion has frequently been interpreted as indicating
abnormalities of the magnocellular system (Cornelissen et al., 1998; Demb, Boynton,
Best, & Heeger, 1998; Hansen et al., 2001; Talcott et al., 1998, however see Skottun,
2000 for a review of contrasting evidence), it is possible that the magnocellular
system could be a common area of deficit in a range of developmental disorders. This
claim has been supported by anatomical evidence of reduced magno-cell size in the
lateral geniculate nucleus of people who have had dyslexia (Livingstone, Rosen,
Drislane, & Galaburda, 1991) and Fragile X syndrome (Kogan et al., 2004). In
addition, it has been reported that the expression of FMRP is higher in magnocellular
neurons than in parvocellular neurons (found in both non-human primate and human
LGNs), suggesting that reduced FMRP associated with Fragile X syndrome may
impact specifically on the development of magnocellular neurons (Kogan et al.,
2004).
Evidence of impaired motion detection in these different developmental
disorders suggests a vulnerability of the magnocellular system / dorsal stream
(Braddick et al. 2003), both in acquired brain damage (Gunn et al., 2002) and
Motion perception and autistic spectrum disorder
19
developmental disorders. A number of speculative suggestions regarding the origin of
such a vulnerability have been put forward including; the physical position of
magnocellular neurons, which makes them more susceptible to compression than
parvocellular neurons (Tassinari, Marzi, Lee, Di Lollo, & Campara, 1999); focal
cortical anomalies which, under certain hormonal conditions, give rise to secondary
disruption in sensory pathways (Ramus, 2004); or a non-specific physical
vulnerability (Gunn et al., 2002). However it is clear from the literature that reduced
sensitivity to coherent motion is not specific to one particular developmental disorder,
neither is it a universal finding in all individuals who have developmental disorders.
As reviewed above, only a proportion of individuals with ASD have abnormally high
motion coherence thresholds (Milne et al., 2002; in press). This appears to be
mirrored in data from children with Williams’ Syndrome (Atkinson et al., 2001), and
also in dyslexia. A meta-analysis of sensitivity to coherent motion revealed that in a
selection of published studies, only 29% of dyslexics had elevated motion coherence
thresholds (Ramus, 2003). An important key to understanding developmental
disorders will be to establish why only sub-groups of individuals with these disorders
have reduced sensitivity to coherent motion, and whether the cause of poor coherent
motion detection is the same in each of the disorders. The normal trajectory of the
development of motion sensitivity may reflect a range of developmental
contingencies, which highlights the possibility that motion perception impairment
may follow rather than precede other cognitive impairments.
There is evidence of abnormal perception of different kinds of motion
amongst individuals with ASD, however in other developmental disorders only
coherent motion detection has been reported as abnormal. This could be because
researchers have not investigated other types of motion perception in other
developmental disorders, although there has been a report of intact biological motion
perception in Williams’ syndrome (Jordan, Reiss, Hoffman, & Landau, 2002), or it
could be that in the other developmental disorders, only coherent motion detection is
impaired and other types of motion stimuli are spared. This suggests that if reduced
sensitivity to coherent motion in ASD shares an underlying aetiology with other
developmental disorders, a further explanation must be sought for the cause of
reduced sensitivity to other types of motion (e.g. biological motion) in ASD. This
work would be enlightened by further investigation of different types of motion
Motion perception and autistic spectrum disorder
20
perception in a range of developmental disorders, and a comprehensive investigation
of different types of motion perception in individuals who have ASD.
A similar issue is the degree to which reduced sensitivity to coherent motion
relates to the varying cognitive profiles of other developmental disorders.
Abnormalities in the magnocellular system have been suggested as causal to poor
reading in individuals with dyslexia, via their input to sub-cortical structures which
control eye-movement (Stein & Walsh, 1997), and a relationship has been found
between sensitivity to coherent motion and reading ability (Cornelissen et al., 1998).
Does this mean that individuals with other developmental disorders who have reduced
sensitivity to coherent motion, will also show reading impairment? A logical
extension of this argument would expect this to be the case. However, recent data
suggests otherwise, as a double dissociation has been found between children with
ASD who have reduced sensitivity to coherent motion but normal reading age and
those who have normal sensitivity to coherent motion and a lower than would be
expected reading age (White et al., in preparation).
Similarly, if it is the case that coherent motion detection is related to global /
local perception via low-spatial frequency processing, then it would be expected that
individuals with dyslexia, Williams’ syndrome and Fragile X syndrome who have
been identified as having high motion coherence thresholds would also show a less
globally biased perceptual style. Given that dyslexics show no abnormality in their
processing of global and local stimuli as indexed by the Navon hierarchical figure
task (Keen & Lovegrove, 2000), this appears not to be the case. However, individuals
with Williams’ syndrome do appear to have a locally biased visuo-motor style which
is shown by their tendency to focus on the local level when asked to reproduce
hierarchical stimuli (Pani, Mervis, & Robinson, 1999).
Conclusions
In conclusion, some individuals with ASD and other developmental disorders
(dyslexia, Williams’ syndrome and Fragile X syndrome) have reduced sensitivity to
visual motion. In ASD this impairment appears to be generalised across many types of
motion (coherent motion, biological motion, response to optic flow and detection of
second-order translational, rotational and radial motion). In other developmental
disorders the impairment appears to be restricted to the detection of coherent motion.
It is not clear whether this reflects a common aetiology across several developmental
Motion perception and autistic spectrum disorder
21
disorders or whether perception of coherent motion is a vulnerable ability which is
diminished in some individuals with developmental disorders. A parallel could be
drawn to IQ, which is generally lower in individuals with developmental disorders,
but is not pin-pointed to a specific aetiology. Available evidence does not yet allow
reliable conclusions regarding the aetiology of impaired motion perception in ASD,
however arguments posited so far have focussed on impairment in a specific area of
the visual system (magnocellular / dorsal stream) and reduced neuronal integration
required for processing complex stimuli.
It remains unclear whether there is a relationship between reduced motion
sensitivity and specific ASD diagnosis. While children with autistic disorder and
Apserger’s syndrome can be differentiated on their postural stability in response to
optic flow (Gepner & Mestre, 2002), high motion coherence thresholds have been
reported in children diagnosed with autistic disorder, Asperger’s Disorder and PDD-
NOS (Milne et al., in press). In addition, a positive relationship between autistic
severity and ability to detect biological motion has been reported by Blake et al.
(2003). It is important for future studies on motion perception in ASD to report the
range of individual differences in the data, and to explicitly illustrate how many
participants with ASD in the sample showed motion perception impairment and how
many showed no impairment. With this approach to the work it is hoped that a clearer
picture will emerge regarding the extent of motion perception impairment in ASD and
the degree to which this is related to other cognitive and / or diagnostic features.
Future Directions
Further understanding the nature of reduced motion sensitivity in individuals
with ASD and other developmental disorders appears to suggest a promising inroad to
a greater understanding not only of the biological architecture and the heterogeneous
nature of ASD, but also of the relationship and over-lap between different
developmental disorders. The phenomenon of motion perception has been studied for
over 50 years, and scientists have made great progress in understanding the functional
anatomy, the psychophysical and also cognitive factors involved in the perception of
motion. Therefore it represents a well-defined model from which to investigate visual
perception in developmental disorders. However, the study of motion perception in
individuals with ASD is a relatively new area in the field and one which will benefit
Motion perception and autistic spectrum disorder
22
from more inclusive, thorough investigation. A number of key issues and further
questions remain outstanding including, but not restricted to:
1) Is reduced sensitivity to motion a general impairment in some individuals with
ASD, that is, are the individuals with ASD who show reduced sensitivity to
coherent motion also the participants who show reduced sensitivity to other
types of motion, e.g. second order motion and/or biological motion?
2) Is there a relationship between reduced sensitivity to motion and ASD
diagnosis and / or between motion perception and symptom severity?
3) Do individuals with developmental disorders other than ASD who show
reduced sensitivity to coherent motion also show deficits in the perception of
other types of motion?
4) Is there direct evidence of abnormal magnocellular neurons in individuals with
ASD?
5) Will functional MRI investigation reveal abnormality in dorsal stream
structures, specifically area V5 during motion perception in individuals with
ASD?
6) Is there direct evidence for reduced neuronal integration across visual motion
areas in individuals with ASD?
References
American Psychiatric Association (1994). Diagnostic and Statistical Manual of
Mental Disorders 4th edition: Washington, DC. American Psychiatric
Association.
Atkinson, J., Anker, S., Braddick, O., Nokes, L., Mason, A. J., & Braddick, F. (2001).
Visual and visuospatial development in young children with Williams
syndrome. Developmental Medicine & Child Neurology, 43, 330 - 337.
Atkinson, J., King, J., Braddick, O., Nokes, L., Anker, S., & Braddick, F. (1997). A
specific deficit of dorsal stream function in Williams' syndrome. Neuroreport,
8, 1919 - 1922.
Avikainen, S., Kulomäki, T., & Hari, R. (1999). Normal movement reading in
Asperger subjects. Neuroreport, 10, 3467 - 3470.
Badcock, J. C., Whitworth, F. A., Badcock, D. R., and , & Lovegrove, W. J. (1990).
Low-frequency filtering and the processing of local-global stimuli. Perception,
19, 617 - 629.
Battelli, L., Cavanagh, P., & Thornton, I. M. (2003). Perception of biological motion
in parietal patients. Neuropsychologia, 41, 1808-1816.
Bavelier, D., Brozinsky, C., Tomann, A., Mitchell, T., Neville, H., & Liu, G. (2001).
Impact of early deafness and early exposure to sign language on the cerebral
organization for motion processing. Journal of Neuroscience, 21, 8931 - 8942.
Motion perception and autistic spectrum disorder
23
Bertone, A., Mottron, L., Jelenic, P., & Faubert, J. (2003). Motion perception in
autism: A "Complex" Issue. Journal of Cognitive Neuroscience, 15, 1 - 8.
Bishop, D. V. M. (1997). Cognitive Neuropsychology and Developmental Disorders:
Uncomfortable Bedfellows. The Quarterly journal of experimental psychology
A, 50(4), 899-923.
Blake, R., Turner, L. M., Smoski, M. J., Pozdol, S. L., & Stone, W. L. (2003). Visual
Recognition of Biological Motion is Impaired in Children with Autism.
Psychological Science, 14(2), 151 - 157.
Boeschoten, M. A., Kemner, C., Kenemans, J. L., & van Engeland, H. (2004).
Abnormal processing of high and low spatial frequencies in autistic children.
Poster presented at the International Meeting for Autism Research,
Sacramento, CA.
Bonda, E., Petrides, M., Ostry, D., & Evans, A. (1996). Specific involvement of
human parietal systems and the amygdala in the perception of biological
motion. Journal of Neuroscience, 16, 3737 - 3744.
Braddick, O., O'Brien, J., Wattam-Bell, J., Atkinson, J., Hartley, T., & Turner, R.
(2001). Brain areas sensitive to coherent visual motion. Perception, 30, 61 -
72.
Brambilla, P., Hardan, A., Ucelli di Nemi, S., Perez, J., Soares, J. C., & Barale, F.
(2003). Brain anatomy and development in autism: review of structural MRI
studies. Brain Research Bulletin, 61, 557 - 569.
Britten, K. H., Shalden, M. N., Newsome, W. T., & Movshon, J. A. (1992). The
analysis of visual motion: A comparison of neuronal and psychophysical
performance. Journal of Neuroscience, 12, 4745 - 4765.
Calvert, G. A., Campbell, R., & Brammer, M. (2000). Evidence from functional
magnetic resonance imaging of crossmodal binding in the human heteromodal
cortex. Current Biology, 10, 649 - 657.
Carlin, M. T., Hobbs, K. L., Bud, M. J., & Soraci, S. A. (1999). Detection of Motion-
defined forms by individuals with mental retardation and autism: Evidence of
modifiability. Intelligence, 27, 141 - 156.
Clifford, C. W. G., & Vaina, L. M. (1999). A computational model of selective
deficits in first and second-order motion processing. Vision Research, 39, 113
- 130.
Cornelissen, P. L., Hansen, P. C., Hutton, J. L., Evangelinou, V., & Stein, J. F.
(1998). Magnocellular visual function and children's single word reading.
Vision Research, 38, 471 - 482.
Cutting, J. E., & Kozlowski, L. T. (1977). Recognition of friends by their walk.
Bulletin of the Psychonomic Society, 9, 353 - 356.
Demb, J. B., Boynton, G. M., Best, M., & Heeger, D. J. (1998). Psychophysical
evidence for a magnocellular pathway deficit in dyslexia. Vision Research, 38,
1555 - 1559.
Derrington, A. M., & Lennie, P. (1984). Spatial and temporal contrast sensitivities of
neurones in the lateral geniculate nucleus of macaque. Journal of Physiology
(London), 251, 483 - 505.
Deruelle, C., Rondan, C., Gepner, B., & Tardif, C. (2004). Spatial Frequency and
Face Processing in Children with Autism and Asperger's Syndrome. Journal
of Autism and Developmental Disorders, 34, 199 - 210.
Fombonne, E. (2003). Epidemiological Surveys of autism and Other Pervasive
Developmental Disorders: An Update. Journal of Autism and Developmental
Disorders, 33, 365 - 382.
Motion perception and autistic spectrum disorder
24
Fox, R., & McDaniel, C. (1982). The perception of biological motion by human
infants. Science, 218, 486 - 487.
Fox, R., & Oross, S. (1990). Mental Retardation and perception of global motion.
Perception and Psychophysics, 48, 252 - 258.
Frith, U. (2003). Autism: Explaining the Enigma (Second ed.). Oxford: Blackwell.
Gepner, B., & Mestre, D. (2002). Brief Report: Postural reactivity to fast visual
motion differentiates autistic children from children with Asperger syndrome.
Journal of Autism and Developmental Disorders, 32, 231 - 238.
Gepner, B., Mestre, D., Masson, G., & De-Schonen, S. (1995). Postural effects of
motion vision in young autistic children. Neuroreport, 6, 1211 - 1214.
Grezes, J., Fonlupt, P., Berenthal, B., Delon-Martin, C., Segebarth, C., & Decety, J.
(2001). Does perception of biological motion rely on specific brain regions?
Neuroimage, 13, 775 - 785.
Grossman, E., & Blake, R. (1999). Perception of coherent motion, biological motion
and form-from-motion under dim-light conditions. Vision Research, 39, 3721-
3727.
Grossman, E., Blake, R., & Kim, C.-Y. (2004). Learning to see Biological Motion:
Brain Activity Parallels Behaviour. Journal of Cognitive Neuroscience, 16,
1669 - 1679.
Grossman, E., Donnelly, M., Price, R., Pickens, D., Morgan, V., Neighbor, G., et al.
(2000). Brain areas involved in perception of biological motion. Journal of
Cognitive Neuroscience, 12, 711 - 720.
Gunn, A., Cory, E., Atkinson, J., Braddick, O., Wattam-Bell, J., Guzzetta, A., et al.
(2002). Dorsal and ventral stream sensitivity in normal development and
hemiplegia. Neuroreport, 13, 843 - 847.
Hansen, P. C., Stein, J. F., Orde, S. R., Winter, J. L., & Talcott, J. B. (2001). Are
dyslexics' visual deficits limited to measures of dorsal stream function?
Neuroreport, 12, 1527 - 1530.
Howard, R. J., Brammer, M., Wright, I., Woodruff, P. W., Bullmore, E., & Zeki, S.
M. (1996). A direct demonstration of functional specialization within motion-
related visual and auditory cortex of the human brain. Current Biology, 6,
1015 - 1019.
Hughes, H. C., Nozawa, G., & Kitterle, F. (1996). Global precedence, spatial
frequency channels and the statistics of natural images. Journal of Cognitive
Neuroscience, 8, 197 - 230.
Jellema, T., Baker, C. I., Wicker, B., & Perrett, D. I. (2000). Neural representation for
the perception of the intentionality of hand actions. Brain and Cognition, 44,
280 - 302.
Johansson, G. (1973). Visual perception of biological motion and a model for its
analysis. Perception and Psychophysics, 14, 201 - 211.
Jordan, H., Reiss, J. E., Hoffman, J. E., & Landau, B. (2002). Intact perception of
biological motion in the face of profound spatial deficits: Williams Syndrome.
Psychological Science, 13, 162 - 167.
Karmiloff-Smith, A. (1998). Development itself is the key to understanding
developmental disorders. Trends in Cognitive Sciences, 2(10), 389-398.
Keen, A. G., & Lovegrove, W. J. (2000). Transient deficit hypothesis and dyslexia:
examination of whole-parts relationship, retinal sensitivity, and spatial and
temporal frequencies. Vision Research, 40, 705 - 715.
Motion perception and autistic spectrum disorder
25
Kogan, C. S., Boutet, I., Cornish, K., Zangenehpour, S., Mullen, K. T., Holden, J. J.
A., et al. (2004). Differential impact of the FMR1 gene on visual processing in
fragile X syndrome. Brain, 127, 591 - 601.
LaGasse, L. (1993). Effects of good form and spatial frequency on global precedence.
Perception and Psychophysics, 53, 89 - 105.
Livingstone, M., & Hubel, D. (1988). Segregation of form, colour, movement and
depth: Anatomy, physiology, and perception. Science, 240, 740 - 749.
Livingstone, M. S., Rosen, G. D., Drislane, F. W., & Galaburda, A. M. (1991).
Physiological and anatomical evidence for a magnocellular deficit in
developmental dyslexia. Proceedings of the National Academy of Science, 88,
7943 - 7949.
Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Leventhal, B. L., DiLavore, P. C., et al.
(2000). The Autism Diagnostic Observation Schedule-Generic: A standard
measure of social and communication deficits associated with the spectrum of
autism. Journal of Autism and Developmental Disorders, 30(205 - 223).
Mather, G., & Murdoch, L. (1997). Order-specific and Non-specific Motion
Responses in the Human Visual System. Vision Research, 37, 605 - 611.
Merigan, W. H., Byrne, C. E., & Maunsell, J. H. (1991). Does primate motion
perception depend on the magnocellular pathway? Journal of Neuroscience,
11, 3422-3429.
Milne, E. (2004). PhD Thesis: "Investigating the correlates of weak central coherence
in autism". University of London (UCL), London.
Milne, E., Swettenham, J., Campbell, R., & Coleman, M. (2004). Degree of global /
local processing is related to coherent motion detection. Paper presented at the
International Meeting for Autism Research, Sacramento, CA.
Milne, E., Swettenham, J., Hansen, P., Campbell, R., Jeffries, H., & Plaisted, K.
(2002). High motion coherence thresholds in children with autism. Journal of
Child Psychology and Psychiatry, 43, 255 - 263.
Milne, E., White, S., Campbell, R., Swettenham, J., Hansen, P., & Ramus, F. (in
press). Motion and Form Coherence Detection in Autistic Spectrum Disorder:
Relationship to Motor Control and 2:4 digit ratio. Journal of Autism and
Developmental Disorders.
Milner, A. D., & Goodale, M. A. (1995). The Visual Brain in Action. New York:
Oxford University Press.
Moore, D. G., Hobson, R. P., & Lee, A. (1997). Components of person perception: an
investigation with autistic, non-autistic retarded and typically developing
children and adolescents. British Journal of Developmental Psychology, 15,
401-423.
Mottron, L., & Belleville, S. (1993). A study of perceptual analysis in a high level
autistic subject with exceptional graphic abilities. Brain and Cognition, 23,
279 - 309.
Mottron, L., Burack, J. A., Iarocci, G., Belleville, S., & Enns, J. T. (2003). Locally
oriented perception with intact global processing among adolescents with
high-functioning autism: evidence from multiple paradigms. Journal of Child
Psychology and Psychiatry, 44, 904 - 913.
Muhle, R., Trentacoste, S. V., & Rapin, I. (2004). The Genetics of Autism. Pediatrics,
113, 472 - 486.
National Autistic Society. (2004). from http://www.nas.org.uk/
Navon, D. (1977). Forest before trees: The precedence of global features in visual
perception. Cognitive Psychology(9), 353 - 383.
Motion perception and autistic spectrum disorder
26
Nealy, T. A., & Maunsell, H. R. (1994). Magnocellular and Parvocellular
contributions to the responses of neurons in Macaque striate cortex. The
Journal of Neuroscience, 14, 2069 - 2079.
Neville, H., J. , & Bavelier, D. (2000). Specificity and Plasticity in Neurocognitive
Development in Humans. In M. S. Gazzaniga (Ed.), The New Cognitive
Neurosciences (2nd ed., pp. 83 - 98). Cambridge MA: The MIT Press.
Neville, H. J., & Lawson, D. (1987). Attention to central and peripheral visual space
in a movement detection task. III. Separate effects of auditory deprivation and
acquisition of a visual language. Brain Research, 405, 284 - 294.
Newsome, W. T., & Pare, E. B. (1988). A selective impairment of motion perception
following lesions of the middle temporal area (MT). Journal of Neuroscience,
8, 2201 - 2211.
O'Neill, M., & Jones, S. P. (1997). Sensory-Perceptual Abnormalities in Autism: A
Case for More Research. Journal of Autism and Developmental Disorders, 27,
283 - 293.
Oram, M. W., & Perrett, D. I. (1994). Responses of anterior superior temporal
polysensory (STPa) neurons to "biological motion" stimuli. Journal of
Cognitive Neuroscience, 6, 99 - 116.
O'Riordan, M., & Plaisted, K. (2001). Enhanced discrimination in autism. The
Quarterly journal of experimental psychology A, 54, 961 - 979.
Pani, J. R., Mervis, C. B., & Robinson, B. F. (1999). Global spatial organization by
individuals with Williams syndrome. Psychological Science, 10, 453 - 458.
Pavlova, M., Krageloh-Mann, I., Sokolov, A., & Birbaumer, N. (2001). Recognition
of point-light biological motion displays by young children. Perception, 30,
925 - 933.
Pavlova, M., Lutzenberger, W., Sokolov, A., & Birbaumer, N. (2004). Dissociable
Cortical Processing of Recognizable and Non-recognizable Biological
Movement: Analysing Gamma MEG Activity. Cerebral Cortex, 14, 181 - 188.
Plaisted, K., Swettenham, J., & Rees, L. (1999). Children with autism show local
precedence in a divided attention task and global precedence in a selective
attention task. Journal of Child Psychology and Psychiatry, 40, 733 - 742.
Puce, A., Allison, T., Bentin, S., Gore, J. C., & McCarthy, G. (1998). Temporal cortex
activation in humans viewing eye and mouth movements. Journal of
Neuroscience, 18, 2188 - 2199.
Puce, A., & Perrett, D. I. (2003). Electrophysiology and brain imaging of biological
motion. Philosophical Transactions of the Royal Society of London B., 358,
435 - 445.
Ramus, F. (2003). Developmental dyslexia: specific phonological deficit or general
sensorimotor dysfunction? Current Opinion in Neurobiology, 13, 212 -218.
Ramus, F. (2004). Neurobiology of dyslexia: A reinterpretation of the data. Trends in
Neurosciences, 27, 720-726.
Rinehart, N. J., Bradshaw, J. L., Moss, S. A., Brereton, A. V., & Tonge, B. J. (2000).
Atypical interference of local detail on global processing in high functioning
autism and asperger's disorder. Journal of Child Psychology and Psychiatry,
41, 769 - 778.
Rogers, S. J., Hepburn, S., & Wehner, E. (2003). Parent Reports of Sensory
Symptoms in Toddlers with Autism and those with Other Developmental
Disorders. Journal of Autism and Developmental Disorders, 33, 631 - 642.
Schenk, T., & Zihl, J. (1997). Visual motion perception after brain damage: II.
Deficits in form-from-motion perception. Neuropsychologia, 35, 1299 - 1310.
Motion perception and autistic spectrum disorder
27
Schiller, P. H., Logothetis, N. K., & Charles, E. R. (1990). Role of colour-opponent
and broad band channels in vision. Visual Neuroscience, 5, 321 - 346.
Schopler, E., Reichler, R. J., & Renner, B. R. (1988). The Childhood Autism Rating
Scale. Los Angeles: Western Psychological Services.
Singh, K. D., Barnes, G. R., Hillebrand, A., Forde, E. M. E., & Williams, A. L.
(2002). Task-Related Changes in Cortical Synchronization Are Spatially
Coincident with the Hemodynamic Response. NeuroImage, 16, 103 - 114.
Skottun, B. C. (2000). The magnocellular deficit theory of dyslexia: the evidence
from contrast sensitivity. Vision Research, 40, 111 - 127.
Smith, A. T., Greenlee, M. W., Singh, K. D., Kraemer, F. M., & Hennig, J. (1998).
The Processing of First- and Second-Order Motion in Human Visual Cortex
Assessed by Functional Magnetic Resonance Imaging (fMRI). Journal of
Neuroscience, 18, 3816 - 3830.
Sparrow, W. A., Shinkfield, A. J., Day, R. H., & Zerman, L. (1999). Visual
perception of human activity and gender in biological motion displays by
individuals with mental retardation. American Journal of Mental Retardation,
104, 215 - 226.
Spencer, J., O'Brien, J., Riggs, K., Braddick, O., Atkinson, J., & Wattam-Bell, J.
(2000). Motion processing in autism: Evidence for a dorsal stream deficiency.
Neuroreport, 11, 2765 - 2767.
Stein, J., & Walsh, V. (1997). To see but not to read; the magnocellular theory of
dyslexia. Trends in Neuroscience, 20, 147 - 152.
Sunaert, S., Van Hecke, P., Marchal, G., & Orban, G. A. (1999). Motion-responsive
regions of the human brain. Experimental Brain Research, 127, 355 - 370.
Talay-Ongan, A., & Wood, K. (2000). Unusual sensory sensitivities in autism: a
possible crossroads. International Journal of Disability, Development and
Education, 47, 201 - 212.
Talcott, J., Hansen, P., Willis-Owen, C., McKinnel, I. W., Richardson, A. J., & Stein,
J. (1998). Visual Temporal Processing in Adult Dyslexics: Evidence for M-
Pathway Dysfunction. NeuroOpthalmology, 20(4), 187 - 201.
Tassinari, G., Marzi, C. A., Lee, B. B., Di Lollo, V., & Campara, D. (1999). A
possible selective impairment of magnocellular function in compression of the
anterior visual pathways. Experimental Brain Research, 127, 391 - 401.
Ungerleider, L. G., & Mishkin, M. (1982). Two cortical visual systems. In D. J. Ingle,
Goodale, M.A., and Mansfield, R.J.W. (Ed.), Analysis of Visual Behaviour
(pp. 549 - 586). Cambridge: MIT Press.
Vaina, L. M., & Cowey, A. (1996). Impairment of the perception of second order
motion but not first order motion in a patient with unilateral focal brain
damage. Proceedings of the Royal Society London B, 263, 1225 - 1232.
Vaina, L. M., & Gross, C. G. (2004). Perceptual deficits in patients with impaired
recognition of biological motion after temporal lobe lesions. Proceedings of
the National Academy of Science, 101, 16947 - 16951.
Vaina, L. M., LeMay, M., Bienfang, D. C., Choi, A. Y., & Nakayama, K. (1990).
Intact Biological Motion and structure from motion perception in a patient
with impaired motion mechanisms. Visual Neuroscience, 5, 353 - 371.
Vaina, L. M., Makris, N., Kennedy, D. N., & Cowey, A. (1998). The selective
impairment of the perception of first order motion by unilateral cortical brain
damage. Visual Neuroscience, 14, 333 - 348.
Motion perception and autistic spectrum disorder
28
Viana, L., Lemay, M., Bienfang, D. C., Choi, A. Y., & Nakayama, K. (1990). Intact
biological motion and structure from motion perception in a patient with
impaired motion mechanisms: A case study. Visual Neuroscience, 5, 353-369.
White, S., Frith, U., Milne, E., Rosen, S., Swettenham, J., & Ramus, F. (in
preparation). Necessary and Sufficient Causes of Reading Disability: A
Comparison of Dyslexic and Autistic Children.
Wong-Riley, M. T. T., Hevner, R. F., Cutlan, R., Earnest, M., Egan, R., Frost, J., N, et
al. (1993). Cytochrome oxidase in the human visual cortex: distribution in the
developing adult brain. Visual Neuroscience, 10, 41 - 58.
Zeki, S. M., Watson, J. D. G., Lueck, C. J., Friston, K., Kennard, C., & Frackowiak,
R. S. J. (1991). A direct demonstration of functional specialization in human
visual cortex. Journal of Neuroscience, 11, 641 - 649.
Zihl, J., Von Cramon, D., Mai, N., & Schmid, C. H. (1983). Disturbance of movement
vision after bilateral posterior brain damage. Brain, 106, 313 - 340.
Motion perception and autistic spectrum disorder
29
Figure one. Schematic Illustration of a random dot kinematogram used to investigate
coherent motion detection.
The stimulus consists of two patches of moving dots. Dots with no arrow indicators
represent dots which move randomly. Dots with arrow indicators represent dots which
move coherently from right to left and left to right. The task is a 2-alternative forced
choice where the participant must detect the patch which contains coherent motion (in
this example, on the left).
Motion perception and autistic spectrum disorder
30
Figure two. Schematic illustration of form detection stimuli.
The stimulus consists of two patches of white lines. In the patch on the right all the
lines are oriented randomly, in the patch on the left some of the lines are oriented to
make a circle. The task is a 2-alternative forced choice where the participant must
detect the coherent form (circle).
Motion perception and autistic spectrum disorder
31
Figure 3. A schematic illustration of a biological motion stimulus (right).
The biological motion display on the right of the figure is composed of point lights
positioned at the joints of the actor. When played as a movie, a strong perception of
walking is apparent solely from the point light display (figure reproduced from Puce
and Perrett, 2003, an adaptation of Johansson, 1973).
Motion perception and autistic spectrum disorder
32
Figure 4. A schematic representation of first and second order translation, radial and
rotational motion (reproduced from Bertone et al, 2003).