Oculomotor studies provide a novel strategy for evaluating the functional integrity of multiple brain systems and cognitive processes in autism. The current study compared pursuit eye movements of 60 high-functioning individuals with autism and 94 intelligence quotient, age and gender matched healthy individuals using ramp and oscillating target tasks. Individuals with autism had normal pursuit latency, but reduced closed-loop pursuit gain when tracking both oscillating and ramp targets. This closed-loop deficit was similar for leftward and rightward pursuit, but the difference between individuals with autism and their age-matched peers was more apparent after mid-adolescence, suggesting reduced maturational achievement of the pursuit system in autism. Individuals with autism also had lower open-loop pursuit gain (initial 100 ms of pursuit) and less accurate initial catch-up saccades during a foveofugal step-ramp task, but these deficits were only seen when targets moved into the right visual field. Pursuit performance in both open- and closed-loop phases was correlated with manual praxis in individuals with autism. Bilateral disturbances in the ability to use internally generated extraretinal signals for closed-loop pursuit implicate frontostriatal or cerebellar circuitry. The hemifield specific deficit in open-loop pursuit demonstrates a lateralized disturbance in the left extrastriate areas that extract visual motion information, or in the transfer of visual motion information to the sensorimotor areas that transform visual information into appropriate oculomotor commands.
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Recent positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) studies in humans have localized the frontal eye field (FEF) to the precentral sulcus (PCS). In macaque monkeys, low-threshold microstimulation and single unit recording studies have located a saccadic subregion of FEF in a restricted area along the anterior wall of the arcuate sulcus and a pursuit subregion located deeper in the sulcus close to the fundus. The functional organization and anatomical location of these two FEF subregions are still to be defined in humans. In the present study, we used fMRI with high spatial resolution image acquisition at 3.0 Tesla to map the saccade- and pursuit-related areas of FEF within the two walls of the PCS in 11 subjects. We localized the saccade-related area to the upper portion of the anterior wall of the precentral sulcus and the pursuit-related area to a deeper region along the anterior wall, extending in some subjects to the fundus or deep posterior wall. These findings localize distinct pursuit and saccadic subregions of FEF in humans and demonstrate a high degree of homology in the organization of these FEF subregions in the human and the macaque monkey.
The ability to anticipate predictable stimuli allows faster responses. The predictive saccade (PRED) task has been shown to quickly induce such anticipatory behavior in humans. In a PRED task subjects track a visual target jumping back and forth between fixed positions at a fixed time interval. During this task, saccade latencies drop from approximately 200 ms to <80 ms as subjects anticipate target appearance. This change in saccade latency indicates that subjects' behavior shifts from being sensory driven to being memory driven. We conducted functional magnetic resonance imaging studies with 10 healthy adults performing the PRED task using a standard block design. We compared the PRED task with a visually guided saccade (VGS) task using unpredictable targets matched for number, direction and amplitude of required saccades. Our results show greater activation during the PRED task in the prefrontal, pre-supplementary motor and anterior cingulate cortices, hippocampus, mediodorsal thalamus, striatum and cerebellum. The VGS task elicited greater activation in the cortical eye fields and occipital cortex. These results demonstrate the important dissociation between sensory and predictive neural control of similar saccadic eye movements. Anticipatory behavior induced by the PRED task required less sensory-related processing activity and was subserved by a distributed cortico-subcortical memory system including prefronto-striatal circuitry.
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