A Positron Emission Tomography Study of Voluntary Saccadic Eye Movements
and Spatial Working Memory.
Sweeney, J.A., M.A. Mintun, S. Kwee, M.B. Wiseman, D.L. Brown, D.R. Rosenberg,
J.R. Carl.
The Neurobehavioral Studies Program, Departments of Psychiatry, Neurology,
Radiology and Ophthalmology, University of Pittsburgh School of Medicine,
Pittsburgh, Pennsylvania, 15213.
APStracts 2:0265N, 1995.
SUMMARY AND CONCLUSIONS
1. The purpose of this study was to define the cortical regions that subserve
voluntary saccadic eye movements and spatial working memory in humans. 2.
Regional cerebral blood flow (rCBF) during performance of oculomotor tasks was
measured with [ 15 O]-H 2 O positron emission tomography (PET). Eleven well-
trained, healthy young adults performed the following tasks: visual fixation,
visually guided saccades, antisaccades (a task in which subjects made saccades
away from rather than toward peripheral targets), and either an oculomotor
delayed response (ODR -- a task requiring memory-guided saccades after a delay
period) or a conditional antisaccade task (a task in which the color of the
peripheral target determined whether a saccade toward or away from the target
was required). An additional six subjects performed a sequential hand movement
task to compare localization of hand-related motor cortex and the frontal eye
fields (FEF), and of the hand and eye movement-related regions of the
supplementary motor area (SMA). 3. Friston's Statistical Parametric Mapping
(SPM) method (Friston et al. 1991) was used to identify significant changes in
rCBF associated with task performance. Since SPM does not take advantage of
the anatomical information available in Magnetic Resonance (MR) scans, each
subject's PET scan was registered to that individual's MR scan, after which
all PET and MR studies were transformed to conform to a standard reference MR
image set. Subtraction images were visually inspected, while overlayed on the
reference MR scan to which PET images had been aligned, in order to confirm
anatomic localization of significant rCBF changes. 4. Compared to visual
fixation, performing visually guided saccades led to a significant bilateral
activation in FEF, cerebellum, striate cortex and posterior temporal cortex.
Right posterior thalamus activation was also observed. 5. The visually guided
saccade task served as the comparison task for the ODR, antisaccade and
conditional antisaccade tasks in order to identify task-related changes in
rCBF beyond those associated with saccade execution. Performance on the ODR
task was associated with a bilateral increase of rCBF in FEF, SMA,
dorsolateral prefrontal cortex (DLPFC), and posterior parietal cortex. The
cortical regions of increased regional blood flow during the ODR task also
showed increased rCBF during the antisaccade task; however, FEF and SMA
activations were significant only in the right hemisphere. These findings
closely parallel those of single cell recording studies with behaving monkeys
in indicating that FEF, DLPFC, SMA and posterior parietal cortex perform
computational activity for voluntary purposive saccades. 6. Comparison of PET
scans obtained during performance of eye movement and hand movement tasks
indicated that peak activations in FEF were located approximately 2 cm lateral
and 1 cm anterior to those of hand-related motor cortex. The oculomotor area
of SMA, the supplementary eye field (SEF), was located approximately 7-8 mm
anterior and superior to the hand-related area of SMA. 7. During performance
of antisaccade and ODR tasks, rCBF was significantly lower in ventromedial
prefrontal cortex, along the rectus gyrus, and in ventral anterior cingulate
cortex than during the visually guided saccade and fixation tasks. During the
antisaccade task, the ventral region of lower rCBF involved medial structures
including left ventral striatum and bilateral medial temporal-limbic cortex.
During the ODR task, the ventral aspect of the region of lower rCBF extended
laterally, rather than medially, to include the temporal poles. The lower
blood flow observed in ventromedial prefrontal cortex (PFC) during both the
antisaccade and ODR tasks, relative to the visually guided saccade and
fixation tasks, suggests that modulation of output from ventromedial PFC to
limbic cortex and the striatum may play a role in the voluntary control of
saccadic eye movements, possibly in the suppression of responses that would
interrupt ongoing purposive behavior. 8. During the ODR task, rCBF changes in
DLPFC, FEF, SMA, posterior parietal cortex, ventral anterior cingulate and
orbital frontal cortex were highly intercorrelated. A similar pattern of
activation across cortical regions was observed during the antisaccade task,
with the exception that activation in SMA was independent from rCBF changes
observed in other cortical regions. These findings suggest that widely
distributed cortico-cortical neural circuitry mediates the voluntary control
of saccades in humans.
Received 24 April 1995; accepted in final form 8 August 1995.
APS Manuscript Number J272-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1995 The American Physiological Society.
Published in APStracts on 23 September 1995.