Positron emission tomography study of voluntary saccadic eye movements and spatial working memory

Abstract

1. The purpose of this study is 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 [15O]-H2O 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 (FEFs) and of the hand- and eye-movement-related regions of the supplementary motor area (SMA). 3. Friston's statistical parametric mapping (SPM) method was used to identify significant changes in rCBF associated with task performance. Because SPM does not take advantage of the anatomic 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 with 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 for identification of 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 FEFs, 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 ...

Spatial maps in frontal and prefrontal cortex

“…This spatial working memory task has been used extensively in studies of monkeys (Funahashi et al, 1989;Sawaguchi and Iba, 2001) and humans (Sweeney et al, 1996), Fig. 4.…”

Cortical and cerebellar activation induced by reflexive and voluntary saccades

“…Numerous functional imaging studies have investigated brain activation related to reXexive or voluntary saccades separately. PET studies have shown activation during reXexive saccades in FEF (Anderson et al 1994;Sweeney et al 1996), PEF (Anderson et al 1994), cerebellum, striate cortex and posterior temporal cortex (Sweeney et al 1996). fMRI studies have also shown activation in FEF (Petit et al 1997;Luna et al 1998;Muri et al 1998; Berman et al Table 2 Areas of activation (voluntary saccades > Wxation) with cluster size, maximum t value within the cluster, MNI coordinates of the maximum t value, anatomic labels, percentage of cluster size and functional area All areas were thresholded at P < 0.05 with FDR (whole brain study) or at cluster level (P < 0.05) corrected for multiple comparisons (cerebellum study) and with a minimum cluster size of 10 voxels L left hemisphere, R right hemisphere, FEF frontal eye Welds, PEF parietal eye Welds, MT/V5 motion-sensitive area (MT/V5), PVA/V1 primary visual areas (V1) a The unassigned areas for each cluster are not listed in the Muri et al 1998;Berman et al 1999;Nobre et al 2000), and the cerebellum (Nobre et al 2000), as well as in SEF (Luna et al 1998;Berman et al 1999), the precuneus , the cingulate gyrus Nobre et al 2000), MT/V5, PVA/V1 and the midbrain.…”

“…Functional imaging studies have shown that the precuneus is involved in reXexive saccadic eye movements and is associated with shifts of spatial attention (Cavanna and Trimble 2006). The anterior cingulate gyrus is involved in target detection (Posner and Petersen 1990) and is activated during self-paced saccades (Paus et al 1993;Petit et al 1996;Sweeney et al 1996) and during reXexive saccades Mort et al 2003). Neurons in the posterior cingulate cortex of primates Wre instantly to assign the spatial coordinates after a saccade in which the eye position signals are provided and to permit monitoring of either eye or self motion (Olson et al 1996).…”

How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades

“…Imaging studies (Sweeney et a!., 1996) have shown thal the frontal cortex is not strongly activated unless the task at hand requires its unique abilities, such as in memory-guided saccadcs or anti-saccades. Taken together, these data suggest a hierarchy of control, such that visual inputs to the SC dominate by default, but the frontal cortex can assume control of the SC when simple reactive eye movements are insuff-Icient ( Figure I).…”