John Wattam-Bell

Motion processing in autism: evidence for a dorsal stream deficiency

We report that motion coherence thresholds in children with autism are significantly higher than in matched controls. No corresponding difference in form coherence thresholds was found. We interpret this as a specific deficit in dorsal stream function in autism. To examine the possibility of a neural basis for the perceptual and motor related abnormalities frequently cited in autism we tested 23 children diagnosed with autistic disorder, on two tasks specific to dorsal and ventral cortical stream functions. The results provide evidence that autistic individuals have a specific impairment in dorsal stream functioning. We conclude that autism may have common features with other developmental disorders and with early stages of normal development, perhaps reflecting a greater vulnerability of the dorsal system.

Brain areas sensitive to coherent visual motion

Detection of coherent motion versus noise is widely used as a measure of global visual-motion processing. To localise the human brain mechanisms involved in this performance, functional magnetic resonance imaging (fMRI) was used to compare brain activation during viewing of coherently moving random dots with that during viewing spatially and temporally comparable dynamic noise. Rates of reversal of coherent motion and coherent-motion velocities (5 versus 20 deg s−1) were also compared. Differences in local activation between conditions were analysed by statistical parametric mapping. Greater activation by coherent motion compared to noise was found in V5 and putative V3A, but not in V1. In addition there were foci of activation on the occipital ventral surface, the intraparietal sulcus, and superior temporal sulcus. Thus, coherent-motion information has distinctive effects in a number of extrastriate visual brain areas. The rate of motion reversal showed only weak effects in motion-sensitive areas. V1 was better activated by noise than by coherent motion, possibly reflecting activation of neurons with a wider range of motion selectivities. This activation was at a more anterior location in the comparison of noise with the faster velocity, suggesting that 20 deg s−1 is beyond the velocity range of the V1 representation of central visual field. These results support the use of motion-coherence tests for extrastriate as opposed to V1 function. However, sensitivity to motion coherence is not confined to V5, and may extend beyond the classically defined dorsal stream.

Dorsal and ventral stream sensitivity in normal development and hemiplegia

Form and motion coherence thresholds can provide comparable measures of global visual processing in the ventral and dorsal streams respectively. Normal development of thresholds was tested in 360 normally developing children aged 4–11 and in normal adults. The two tasks showed similar developmental trends, with some greater variability and a slight delay in motion coherence compared to form coherence performance, in reaching adult levels. To examine the proposal of dorsal stream vulnerability related to specific developmental disorders, we compared 24 children with hemiplegic cerebral palsy with the normally developing group. Hemiplegic children performed significantly worse than controls on the motion coherence task for their age, but not on the form coherence task; however, within this group no specific brain area was significantly associated with poor motion compared to form coherence performance. These results suggest that extrastriate mechanisms mediating these thresholds normally develop in parallel, but that the dorsal stream has a greater, general vulnerability to early neurological impairment.

Changes in Infants' Ability to Switch Visual Attention in the First Three Months of Life:

The abilities of 1-month-old and 3-month-old infants to shift their gaze from a central target to a peripheral target were compared in four experiments. In experiment 1 targets matched in mean luminance to the background were presented to infants in the periphery at varying levels of contrast. The contrast thresholds for target detection were found to be significantly different for 1-month-olds compared with 3-month-olds. With targets set close to these contrast thresholds, correct refixations and the latency for shifting attention were examined in experiment 2. Two conditions were used: a peripheral target was presented against a homogeneous background (noncompetition); and in the second condition, the patterned target appeared at one of two lighter peripheral windows set against a darker background (competition). Although there was no difference between the two age groups in the latency for shifting visual attention, 1-month-olds were found to make more directional errors in the competition condition. The competition effect of two potential targets on latencies was examined in experiment 3. In the competition condition, two identical peripheral patterned targets were presented to the infants. The 3-month-olds refixated more quickly to one of the double targets in the competition condition than to a single peripheral target, whereas 1-month-olds were slowed down by a double target display. Finally, in experiment 4 the ability of the infants to process and disengage from a central stimulus and to refixate towards a similar peripheral target was examined. This type of competition disrupted both the direction of the first eye movement and the latency to shift attention in both age groups. However, the effect was significantly greater for the 1-month-olds. Taken together, the results of these experiments demonstrate the greater disruption of fixation-shift behaviour in 1-month-olds compared with 3-month-olds when competing visual stimuli are used. This developmental change is explained in terms of maturation of executive cortical orienting systems over the first months of life.

Development of motion-specific cortical responses in infancy

The development of visual motion mechanisms has been studied in infants with a visual evoked potential (VEP) technique which isolates responses from directionally-selective mechanisms. In adults, the amplitude of this directional VEP increased with velocity up to a maximum at 15-20 deg/sec, and then declined with further increases in velocity. In a group of infants tested longitudinally, directional responses were first found at a median age of 74 days with a stimulus velocity of 5 deg/sec, and 90 days with a velocity of 20 deg/sec; this age difference was statistically significant. Initially, VEP amplitudes were significantly greater at 5 deg/sec than at 20 deg/sec. By the end of the longitudinal study, there was no significant difference in amplitudes at the two velocities. In a second group of infants, simultaneous recording of VEPs and electrooculograms indicated that eye movements tracking the stimulus were not a significant factor in the development of the directional VEP. It is concluded that the development of directional selectivity starts at low velocities, and extends to higher velocities with age.

Development of Orientation Discrimination in Infancy

It has previously been found by us, with a visual evoked potential (VEP) measure, that orientation discrimination of dynamic patterns in infants can be demonstrated from around 6 weeks after birth. Experiments are reported in which orientation discrimination was measured behaviourally, in two infant control habituation procedures, with both dynamic and static patterns. When dynamic patterns identical to those in our previous VEP studies were used, the first positive evidence of orientation discrimination was found at around 6 weeks postnatally. The time course of both the VEP and the behavioural measures was similar. However, with static patterns, evidence of orientation discrimination by newborns was found if the infants were allowed to compare the habituated and novel orientations in a paired simultaneous comparison after habituation, but was not found when the habituated and novel stimulus were presented sequentially. The positive evidence of orientation discrimination in newborns supports the hypothesis that some form of orientationally tuned detectors can be used for discrimination of static patterns at birth. However, some developmental change over several weeks seems to be required before a positive electrophysiological VEP response can be measured for dynamic patterns changing in orientation.

Dorsal-stream motion processing deficits persist into adulthood in Williams syndrome

Previous studies of children with Williams syndrome (WS) have found a specific deficit in dorsal cortical stream function, indicated by poor performance in coherence thresholds for motion compared to form. Here we investigated whether this is a transient developmental feature or a persisting aspect of cerebral organization in WS. Motion and form coherence thresholds were tested in a group of 45 WS individuals aged 16-42 years, and 19 normal adult controls. Although there was considerable variation in the coherence thresholds across individuals with WS, the WS group showed overall worse performance than controls. A significant group x threshold condition interaction showed a substantially greater performance deficit for motion than for form coherence in the WS group relative to controls. This result suggests that the motion deficit is an enduring feature in WS and is a marker for one aspect of dorsal-stream vulnerability.

The development of maximum displacement limits for discrimination of motion direction in infancy.

The development of visual motion mechanisms has been studied in infants by using forced-choice preferential looking to measure maximum displacement limits (dmax) for the detection of coherent motion in random-dot patterns. The motion consisted of a sequence of coherent displacements at intervals of 20 msec. Between 8 and 15 weeks, dmax for discrimination of coherent from incoherent motion, and for discrimination of opposite directions of coherent motion, increased with age; in both conditions, dmax for the oldest infants was less than a third of the value found in adults. For 10-11-week-old infants, and for an adult subject, reducing stimulus contrast from 88 to 48% had no effect on dmax for direction discrimination, which indicates that the rise in dmax with age is not simply a result of improving contrast sensitivity. When the displacement interval was increased from 20 to 40 msec, dmax increased significantly in 8-11-week-olds, but remained unchanged in 12-15-week-olds. These results show that while directional mechanisms are present in the visual system by 8 weeks, they operate over a restricted velocity range. The upper limit of this velocity range increases with age. After about 12 weeks, the increase is mainly due to changes in the spatial properties of motion mechanisms; however, in younger infants changes in their temporal properties are also important.

Visual motion processing in one-month-old infants: Preferential looking experiments

The ability of infants to discriminate between opposite directions of motion was assessed using forced-choice preferential looking between a random-dot pattern which was segregated into regions which moved in opposite directions, and a uniform pattern in which all the dots moved in the same direction. The first experiment measured velocity thresholds (Vmin and Vmax) for direction discrimination; between 10 and 13 weeks Vmin decreased, while at the same time Vmax increased. The second experiment explored possible implications of this expanding velocity range for direction discrimination by younger infants. One-month-olds showed no evidence for direction discrimination at any of a number of test velocities in the range 1-43 deg/sec. The 1-month-olds were also tested with two additional conditions: they could discriminate between moving and static patterns at velocities of 10 deg/sec or above, and they could also discriminate between coherent and incoherent motion at velocities of 21 deg/sec or below. Neither of these discriminations depends on sensitivity to the direction of the coherent motion. The results suggest that 1-month-olds may not be sensitive to the direction of visual motion.

Motion- and orientation-specific cortical responses in infancy.

During the first 3 months, infants develop visual evoked potential (VEP) responses that are signatures of cortical orientation-selectivity and directional motion selectivity. Orientation-specific cortical responses develop in early infancy. This study compared these responses directly in the same infants, to investigate whether the later appearance of direction selectivity was intrinsic, or a function of the spatio-temporal characteristics of the stimuli used. Steady-state orientation-reversal (OR-) VEPs and direction-reversal (DR-) VEPs were recorded in infants aged 4-18 weeks. DR-VEPs were elicited with random pixel patterns and with gratings spatially similar to those used for OR-VEPs, at velocities of 5.5 and 11 deg/s, and reversal rates of 2 and 4 reversals/s. Infants throughout the age range showed significant responses to orientation-reversal. Direction-reversal responses appeared in less than 25% of infants under 7 weeks of age, rising to 80% or more at 11-13 weeks, whether tested with dots or gratings and for both speeds and reversal rates. However, 2 reversals/s elicits the DR-VEP on average about 2 weeks earlier than 4 reversal/s stimulation. We conclude that human cortical direction selectivity develops separately from orientation-selectivity and emerges at a later age, even with tests that are designed to optimise the former.