Autism is a genetic disorder that is associated with impairments in sensorimotor behaviorsas well as deficits in language, cognition and social skills. Impairments in postural control (Minshew et al., 2004
; Molloy et al., 2003
), eye movements (Goldberg et al., 2002
; Luna et al., 2007
; Takarae et al., 2004a
)and motor learning (Mostofsky et al., 2000
; Müller et al., 2004
; Rinehart et al., 2001
)all have been reported in autism . Sensorimotor functions are supported by extensive cortical and subcortical networks. Because the neuroanatomy of sensorimotor systems are well understood, and sensory inputs and motor responses are more easily quantifiable than most higher cognitive processes, an examination of sensorimotor behaviors offers advantages to investigate what neural circuits are selectively affected in autism.
While sensorimotor impairments have been reported in autism, it is not clear whether sensorimotor deficits in autism are primarily consequences of altered sensory input to sensorimotor systems, or result from intrinsic disturbances in sensorimotor systems themselves. For example, smooth pursuit eye movements, which maintain visual focus on moving objects, depend on the analysis of visual motion information and are initiated in response to visual movement (Ilg, 1997
; Newsome et al., 1985
). The emergence of smooth pursuit during development follows maturation of the extrastriate area MT that is dedicated to visual motion processing (Johnson, 1990
), suggesting a closely coordinated timing in maturation in the abilities to perceive and respond to visual motion signals.
Several studies have reported impairments in visual pursuit in autism. Scharre and Creedon (Scharre & Creedon, 1992
)and Rosenhall and colleagues (Rosenhall et al., 1988
) reported difficulty inducing smooth pursuit in subjects with autism. Though the latter reported some normalization of pursuit accuracy once smooth pursuit was successfully induced, lack of pursuit responses in most subjects points to abnormality in the pursuit system. Kemner and others (Kemner et al., 2004
)studied smooth pursuit eye movements in 14 children with Pervasive Developmental Disorders (PDD) and 14 age and IQ matched control children. While not statistically significant, they reported about a 10% reduction in pursuit gain (pursuit velocity relative to target velocity) in the PDD group. Takarae and colleagues(Takarae et al., 2004a
) found pursuit impairments in 60 high-functioning individuals with autism compared to 94 age and IQ matched typically developing control subjects. They reported unidirectional impairments during pursuit to the right during the initiation of smooth pursuit and bidirectional impairments in sustained pursuit driven by predictive signals.
Pursuit impairments in autism might be caused by disturbances in visual processing as past studies have reported impairments in visual motion perception in autism (Bertone et al., 2003
; Milne et al., 2002
; Spencer et al., 2000
). The degree to which impairments in visual perception explain visual sensorimotor deficits in autism is, however, not clear. Our past work documented significant correlations between pursuit performance and manual motor skills in autism (Takarae et al., 2004a
), suggesting that visual pursuit impairments might be part of more general visual sensorimotor or motor impairments. Milne et al. (Milne et al., 2006
)reported abnormally high motion detection thresholds in only 22% of their participants, and whether or not individuals with more severe motion perception impairments have more severe pursuit impairments remains to be established. There is potential heterogeneity with respect to the development of sensorimotor and sensory brain systems in autism, in which each system could be more or less impaired to result in general sensorimotor disturbances.
The current study examined visual motion perception, visual pursuit, manual motor control, and relationships between these behavioral domains in autism. We used two different visual pursuit tasks because some aspects of visual pursuit are more sensitive to the quality of visual sensory input to the oculomotor system than others. Lesions in the area MT most profoundly affect latency of pursuit eye movements and pursuit gain during the initial 100 msec from the onset of smooth pursuit (referred to as the open-loop stage) (Dursteler & Wurtz, 1988
; Newsome et al., 1985
). Thus, we used two different paradigms to examine pursuit initiation and maintenance separately. We also employed two different paradigms to examine visual motion processing because previous literature has suggested that performance on visual motion tasks can depend on stimulus characteristics (Bertone et al., 2003
). One task was a motion coherence task which requires integration of local motion vectors to compute global motion, and the other was based on detecting moving gratings which could be performed by detection of local motion alone. Because we previously found lateralized impairments during pursuit initiation, we assessed performance in the left and right hemifield separately during visual pursuit and visual motion tasks. To our knowledge, this is the first study that examined visual motion perception in each hemifield separately in autism. We also used neuropsychological measures of manual motor skills to replicate our previous findings of a relationship between manual motor skills and visual pursuit performance and to assess the generality of sensorimotor deficits across visuomotor systems.
Because of previous findings indicating that visual perception may be differentially affected in high-functioning autism and Asperger’s Disorder (Spencer & O'Brien, 2006
), we divided participants meeting the Autism Diagnostic Interview-Revised (ADI-R) and the Autism Diagnostic Observation Schedule (ADOS) criteria for autism according to their history of early language development. That is one of critical factors differentiating the two clinical disorders. A diagnosis of Asperger’s Disorder requires the absence of delayed language development, whereas DSM-IV criteria for Autistic Disorder do not require delayed language development. Thus, one could have a diagnosis of Autistic Disorder regardless of the presence or absence of delayed language development. In DSM-IV, diagnosis of Autistic Disorder supercedes Asperger’s Disorder, and thus the difference between two disorders reflects both qualitative and quantitative differences. In the current study, we compared two autism groups with similar symptom severity measures on the ADOS rating scale.
Defining subgroups of individuals with autism based on language development has been proposed as a viable phenotype in autism by genetic and brain imaging studies as well as behavioral analysis( Tager-Flusberg & Joseph, 2003), and those with language delay might have specific genetic alterations(Alarcon et al., 2002
; Bradford et al., 2001
) . Our previous work on saccadic eye movements documented that autism groups that were defined by the presence or absence of early language delay were associated with a distinct pattern of neurophysiological impairments (Takarae et al., 2004b
). Delay in language acquisition likely represents an observable clinical marker for changes in complex brain maturation at the age that early language skills are acquired; these have diverse implications for many neuropsychological processes. Effects involving language development and visual processing might occur via alteration in the superior temporal sulcus or its white matter connections that are implicated in autism and are associated with both verbal abilities and high-level visual processing (Redcay, 2008
; Zilbovicius et al., 2006
). In the present study, we examined whether problems in early language acquisitionare related to impairments in visual pursuit and visual motion perception.