Coherent motion processing in autism spectrum disorder (ASD): An fMRI study

Abstract

A deficit in global motion processing caused by a specific dysfunction of the visual dorsal pathway has been suggested to underlie perceptual abnormalities in subjects with autism spectrum disorders (ASD). However, the neural mechanisms associated with abnormal motion processing in ASD remain poorly understood. We investigated brain responses related to the detection of coherent and random motion in 15 male subjects with ASD and 15 age- and IQ-matched healthy controls (aged 13–19 years) using event-related functional magnetic resonance imaging (fMRI). Behaviorally, no significant group differences were observed between subjects with ASD and controls. Neurally, subjects with ASD showed increased brain activation in the left primary visual cortex across all conditions compared with controls. A significant interaction effect between group and condition was observed in the right superior parietal cortex resulting from increased neural activity in the coherent compared with the random motion conditions only in the control group. In addition, neural activity in area V5 was not differentially modulated by specific motion conditions in subjects with ASD. Functional connectivity analyses revealed positive correlations between the primary visual cortex and area V5 within both hemispheres, but no significant between-group differences in functional connectivity patterns along the dorsal stream. The data suggest that motion processing in ASD results in deviant activations in both the lower and higher processing stages of the dorsal pathway. This might reflect differences in the perception of visual stimuli in ASD, which possibly result in impaired integration of motion signals.

Introduction

Autism spectrum disorders (ASD) are neurodevelopmental disorders characterized by impairments in social communication and interaction as well as repetitive, stereotyped behaviors. An additional non-social feature of autism is sensory abnormality (Rogers & Ozonoff, 2005). Heightened sensitivity to small differences between stimuli, increased attention to fragments or surface features of objects, and a relative failure to extract the information context have been described frequently in autistic individuals (Dakin and Frith, 2005, Hill and Frith, 2003). This information processing style, characterized by favoring local over global feature aspects, is specific to autism (Bertone & Faubert, 2006) and could explain both impaired and superior perceptual processing in ASD (Happé & Frith, 2006).

Recently, there has been a growing interest in low-level perceptual processing in ASD especially in the visual domain, but the neural basis of these abnormalities is still unknown. Furthermore, different theories suggest that abnormal visual processing in ASD is characterized by an integration deficit at an early stage of visual processing and/or a dysfunction of the visual pathways (Bertone et al., 2005, Davis et al., 2006, Happé and Frith, 2006).

The visual system beyond the primary visual cortex segregates into at least two streams, the dorsal and ventral pathways, each of which processes and transmits the information about objects and events in different ways and for different purposes (Goodale and Milner, 1992, Livingstone and Hubel, 1987). The ventral stream projects from the primary visual cortex to area V4 to the inferotemporal cortex. It is mainly responsible for the perceptual identification of objects, and it receives input from the parvocellular system for high spatial frequencies. The dorsal pathway on the other hand projects from the striate cortex to the middle temporal area (MT/V5) to the posterior parietal cortex. It receives input mainly from the magnocellular layers of the lateral geniculate nucleus (LGN), which are sensitive to low spatial frequencies, and it plays an important role in the localization of visual stimuli and the control of object-related actions towards an object (Goodale and Milner, 1992, Milner and Goodale, 2008). Notably, the cells in the dorsal stream, especially in MT/V5, are highly responsive to motion stimuli (Culham et al., 2001, Tootell et al., 1995). A classical psychophysical task for investigating the function of this pathway is coherent motion detection (Braddick et al., 2001, Newsome and Pare, 1988), in which the perception threshold of an observer is measured by determining the lowest proportion of dots that is needed to correctly identify the direction of coherent motion in a stimulus patch (Dakin & Frith, 2005). Functional imaging studies have shown that in healthy subjects, coherent motion stimuli compared with static or random motion stimuli, activate the specialized motion-sensitive area MT/V5 along with other occipital and parietal areas (Braddick et al., 2001, Culham et al., 2001).

In autism, several behavioral studies have reported increased motion coherence thresholds or motion-processing deficits, although this pattern could not consistently be replicated across all studies (Del Viva et al., 2006, Milne et al., 2006, Vandenbroucke et al., 2008b), in particular no group differences were found if IQ differences were controlled (Koldewyn, Whitney, & Rivera, 2009). At the neural level, a disturbed dorsal pathway for motion processing, despite an intact ventral pathway for form processing, has been suggested to reflect a dorsal stream vulnerability in neurodevelopmental disorders (Braddick, Atkinson, & Wattam-Bell, 2003). Furthermore, Milne et al. (2002) interpreted abnormally high motion coherence thresholds in relation to the local processing bias in ASD by postulating that both are a consequence of low levels of activity in the low spatial frequency channels of the magnocellular pathway, which possibly lead to abnormal development of the parietal lobe. Contrary to this hypothesis, other researchers have reported intact lower level dorsal stream functioning (processed in the primary visual cortex) and suggested that second-order or coherent motion-processing deficits in autism stem from a higher order deficit in the integration of ‘complex’ information at the global level instead of a motion-processing deficit per se (Bertone et al., 2003, Pellicano et al., 2005). Hence, the motion-sensitive area V5 might be responsible for increased motion thresholds in ASD. This region is crucial for motion processing in the brain, and at this stage, local directional signals are combined to form a global percept, which involves additional cooperative mechanisms in the cortex (Braddick et al., 2001). Furthermore, neural responses in V5 have shown a linear dependence on increasing coherence levels (Rees, Friston, & Koch, 2000).

Recently, it has also been suggested that perceptual deficits in ASD are not only due to dysfunctions within a specific pathway or region but are rather related to reduced connectivity between distant brain regions that might lead to a reduced top–down modulation of lower level sensory processing (Just et al., 2007, Just et al., 2004, Koshino et al., 2005, Villalobos et al., 2005), but non-replications are puzzling (for review: Muller, 2008). Thus, the exact neural mechanism underlying deficits in motion processing have yet to be elucidated. In particular, it remains unclear at which stage of information processing deficits occurs.

In the present functional magnetic resonance imaging (fMRI) study, we used a coherent motion detection task that reliably activates the dorsal visual stream to investigate the neural mechanisms underlying abnormal motion processing in ASD in comparison with a healthy control group. This kind of task exemplifies early neurointegrative processing and is mediated mainly by area MT/V5, which is a specialized motion-sensitive region in extrastriate cortex (Braddick et al., 2001). On the basis of behavioral coherent motion studies in ASD, we hypothesized that the neural activity of the motion-sensitive region MT/V5 is abnormal in subjects with ASD compared with controls. Since previous neuroimaging studies in autism also reported increased activation in early visuo-perceptual processing areas (Manjaly et al., 2007), but reduced neural activity in “higher order” cortical regions (Mottron, Dawson, Soulieres, Hubert, & Burack, 2006), we conducted a whole-brain imaging analysis to examine the extent to which higher order or early perceptual differences are involved in abnormal visual processing in ASD. Moreover, the functional connectivity among activated areas of the dorsal motion pathway were investigated to further test the hypothesis that deficits in the integration of complex information in ASD are associated with abnormal coupling between these brain regions.