Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda, Maryland 20892
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Petit, Laurent and James V. Haxby. Functional Anatomy of Pursuit Eye Movements in Humans as Revealed by fMRI. J. Neurophysiol. 82: 463-471, 1999. We have investigated the functional anatomy of pursuit eye movements in humans with functional magnetic imaging. The performance of pursuit eye movements induced activations in the cortical eye fields also activated during the execution of visually guided saccadic eye movements, namely in the precentral cortex [frontal eye field (FEF)], the medial superior frontal cortex (supplementary eye field), the intraparietal cortex (parietal eye field), and the precuneus, and at the junction of occipital and temporal cortex (MT/MST) cortex. Pursuit-related areas could be distinguished from saccade-related areas both in terms of spatial extent and location. Pursuit-related areas were smaller than their saccade-related counterparts, three of eight significantly so. The pursuit-related FEF was usually inferior to saccade-related FEF. Other pursuit-related areas were consistently posterior to their saccade-related counterparts. The current findings provide the first functional imaging evidence for a distinction between two parallel cortical systems that subserve pursuit and saccadic eye movements in humans.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Visually guided eye movements are of two distinct
types, saccadic and smooth pursuit (Dodge 1903). The
primary function of the saccadic system is to orient gaze to visual
targets for foveal viewing, whereas the function of the pursuit system
is to maintain visual targets within the fovea when either the stimulus
or the individual is in motion.
Elements of the neurophysiological and anatomic organization of both
the saccadic and pursuit systems have been identified in nonhuman
primate studies (for review see Eckmiller 1987;
Keller and Heinen 1991
; Leigh and Zee
1991
; Wurtz and Goldberg 1989
). In particular,
neurophysiological studies in monkeys have differentiated saccade- and
pursuit-related neural activity in various cortical regions, including
the frontal eye field (FEF) (Gottlieb et al. 1993
, 1994
;
McAvoy et al. 1991
; Tian and Lynch
1996a
), the supplementary eye field (SEF) (Heinen
1995
; Tian and Lynch 1995
), and the
intraparietal sulcus (IPS) (Bremmer et al. 1997a
;
Colby et al. 1993
). Further, pursuit-related activity
has been described in the monkey middle temporal (MT) and medial
superior temporal (MST) areas in the superior temporal sulcus
(Bremmer et al. 1997b
; Komatsu and Wurtz 1988
).
Numerous clinical (e.g., for review Pierrot-Deseilligny et al.
1995) and functional brain imaging studies [positron emission tomography (PET)] (Anderson et al. 1994
; Fox et
al. 1985
; Kawashima et al. 1996
;
O'Driscoll et al. 1995
; O'Sullivan et al.
1995
; Paus et al. 1993
; Sweeney et al.
1996
) and functional magnetic resonance imaging (fMRI)
(Darby et al. 1996
; Luna et al. 1998
;
Müri et al. 1996
; Petit et al.
1997a
) have consistently demonstrated that the FEF, SEF, and
IPS (also referred to as the parietal eye field, PEF) constitute the
dorsal cortical areas subserving visually guided saccades in humans.
Clinical studies have described smooth pursuit deficits related to
lesions in cortical regions overlapping the FEF, SEF, and PEF but have
also indicated a role for the lateral occipitotemporal cortex (the
monkey MT/MST-homologous areas) (Heide et al. 1996; Morrow and Sharpe 1993
, 1995
; Pierrot-Deseilligny
1994
). In contrast to functional imaging studies of saccadic
eye movements, little attempt has been made to use PET or fMRI to
explore the functional anatomy of pursuit eye movements in healthy
humans. Only one published fMRI study has described the activation of
the lateral occipitotemporal cortex during smooth pursuit
(Barton et al. 1996
). To our knowledge, there is no
published report of activation of frontal and parietal areas during
pursuit eye movements in healthy humans. Aside from our preliminary
report on FEF activation in the current study (Petit et al.
1997a
), previous frontal and parietal pursuit-related activations have been reported only in abstract form (Berman et al. 1996
; Brandt et al. 1997
; Colby and
Zeffiro 1990
; Sweeney et al. 1998
).
The aim of this study was to investigate the functional anatomy of pursuit eye movements with fMRI. Subjects were instructed to follow a visual dot moving back and forth across the horizontal axis with a constant velocity. In addition to the involvement of the occipitotemporal cortex during pursuit, we predicted that the location of pursuit-related activity would lie within the dorsal cortical areas involved in the execution of visually guided saccades, namely the FEF, SEF, and PEF. Subjects also performed a visually guided saccade task to identify the saccade-related dorsal cortical areas and to test the possible existence of two functional subregions, one for the pursuit and one for the saccadic eye movements, in FEF, SEF, and PEF.
Preliminary results from this study have appeared previously in
abstract form (Petit et al. 1997b) and in a short report
on FEF activation (Petit et al. 1997a
).
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Subjects
Five healthy right-handed volunteers (2 males, 3 females, mean age 23.8 ± 4.1 yr) participated in this study. All were free of neurological or psychiatric illness, and there were no abnormalities on their structural magnetic resonance images. All subjects gave written, informed consent.
Task design
fMRI scans were obtained while subjects alternately performed either pursuit or visually guided saccadic eye movements and baseline control tasks. During the pursuit task, subjects were asked to follow a visual dot starting at the primary central eye position and moving back and forth across the horizontal axis with a constant speed of 25°/s and with a maximal amplitude of 12° on both sides. During the saccadic task, subjects were asked to execute saccadic eye movements toward a visual dot. The dot appeared first at the primary central eye position for 500 ms and then jumped randomly to different eccentric positions on the horizontal axis with a frequency of 2 Hz. The number of left and right saccadic eye movements were equated, with an average amplitude of 12° in both directions (range, 5-20°). The visual dot size was 0.4°. During the control task, subjects were in total darkness and were asked to keep their eyes open and to avoid moving their eyes.
Visual targets were generated by a Power Macintosh computer (Apple;
Cupertino, CA) with SuperLab (Cedrus; Wheaton, MD) (Haxby et al.
1993) and were projected with a magnetically shielded liquid crystal display video projector (Sharp; Mahwah, NJ) onto a translucent screen placed at the feet of the subject. The subject was able to see
the screen by the use of a mirror system. An RK-416PC pupil infrared
eye tracking system (ISCAN; Cambridge, MA) was used to record the
subject's eye movements outside the magnet to ascertain that the
subject correctly understood the oculomotor tasks. Figure 1A illustrates a subject's
eye position during the performance of the pursuit task and during the
execution of horizontal saccadic eye movements.
|
Imaging procedure
All imaging used a 1.5 T GE Signa magnet (Milwaukee, WI) with a standard head coil. Interleaved multislice gradient echo echo-planar imaging (EPI) was used to produce 26 contiguous, 5-mm thick axial slices covering the entire brain [repetition time (TR) = 3,000 ms; echo time (TE) = 40 ms, flip angle 90°, field of view = 24 cm, 64 × 64 matrix, voxel dimensions = 3.75 × 3.75 × 5 mm]. Each subject performed four series contrasting saccade and control tasks and four series contrasting pursuit and control tasks, counterbalanced across subjects. For each series, subjects alternated 15 s of a control task and 15 s of an oculomotor task. Each series consisted of 60 scans with a complete duration of 3 min. The scanner was in the acquisition mode for 12 s before each series to achieve steady-state transverse magnetization.
For all studies, high-resolution volume spoiled gradient recalled echo structural 2.5-mm thick axial images were also acquired at the same locations as the EPIs (TR = 13.9 ms, TE = 5.3 ms, flip angle 30°) to provide detailed anatomic information.
Data analysis
The fMRI time series data were analyzed with multiple regression
(Haxby et al. 1998). Activity related to smooth pursuit
and visually guided saccades was contrasted independently, relative to
activity during the control task. Both contrasts were constructed a
priori such that the sum of values over the time series equals zero and
the cross products of all pairs of contrasts are equal to zero,
demonstrating orthogonality. Each of the time series was convolved with
a Gaussian model of the hemodynamic response to produce the two
regressors used in the analysis. The same parameters for the Gaussian
model were applied to all voxels (lag = 4.8 s, dispersion = 1.8 s) (Maisog et al. 1995
).
Multiple regression simultaneously calculates a weighting coefficient
for each regressor such that the sum of two regressors multiplied by
their weighting coefficient provides the best fit to the data. All
statistical results have a single voxel Z threshold of 2.33 (degrees of freedom corrected for correlation between adjacent time
points). Statistical significance (P < 0.05) of a
region of activation was determined with an analysis based on the
spatial extent of each region to correct for multiple comparisons
(Friston et al. 1994
). For each subject,
z-score maps and structural images were transformed into the
standard stereotactic Talairach space (Talairach and Tournoux 1988
) with the three-dimensional version of SPM (Friston
1995
).
Activated voxels in three bilateral and two midline volumes of interest (VOIs, Fig. 1B) were analyzed for the location and spatial extent of the FEF (precentral cortex), the SEF (medial superior frontal cortex), PEF (intraparietal sulcus), MT/MST (the lateral junction of the occipital and temporal cortex), and the precuneus. By using the Talairach normalized structural images, this parcellation was achieved for each subject with software (Voxtool; General Electric; Buc, France) designed for brain segmentation, reconstruction of the external surfaces of both hemispheres, and display of sections in any orientation.
The VOI delineating bilateral precentral regions encompassed the
precentral gyrus and the precentral sulcus, including 5 mm on the
anterior bank of the sulcus from the junction with the superior frontal
sulcus to the lateral convexity. Its inferior limit corresponded to the
plane 30 mm above the bicommissural plane (AC-PC). This inferior limit
was chosen to delineate the part of the precentral cortex that contains
the FEF (Luna et al. 1998; Paus 1996
).
The VOI delineating the dorsomedial part of the superior frontal gyrus
consisted of 15 mm of cortex on each side of the interhemispheric fissure anterior to the vertical plane passing through the posterior commissure (VPC) and extending forward to the anterior convexity. Its
inferior limit corresponded to the cingulate sulcus in the posterior
part and to the plane 45 mm above AC-PC in the anterior part. This
inferior limit was chosen to delineate the medial part of Brodmann's
area 6 that contains both the supplementary motor area and the SEF
(Picard and Strick 1996).
The VOI delineating bilateral intraparietal sulcal regions (IPS) included the cortex on both banks of the sulcus, namely both superior and inferior parietal lobules, from the junction with the postcentral sulcus to the posterior convexity. Its inferior limit corresponded to the plane 30 mm above the AC-PC plane and thus included the deepest part of the intraparietal sulcus. The term IPS is used to refer to the anatomically defined VOI, and the term PEF is used to refer to the part of IPS that is involved in eye movements.
The VOI delineating bilateral regions at the lateral junction of the
temporal and occipital cortex was centered on the junction of the
ascending limb of the inferior temporal sulcus and the lateral
occipital sulcus. Its anterior limit corresponded to the coronal plane
40 mm posterior to the VAC plane and extending backward to the coronal
plane 85 mm posterior to the VAC. Its superior limit corresponded to
the plane 12 mm above the AC-PC plane, and its inferior limit
corresponded to the plane 4 mm below the AC-PC plane. This region was
defined to include the area that is homologous to monkey MT/MST, also
called V5 (Tootell et al. 1995; Watson et al.
1993
; Zeki et al. 1991
). The lateral junction of
the temporal and occipital cortex refers to the anatomically defined
VOI, and the term MT/MST refers to the functionally defined part of
that cortex.
The VOI delineating the precuneus consisted of 15 mm of parietal cortex on each side of the interhemispheric fissure, posterior to the marginal ramus of the cingulate sulcus and extending backward to the posterior convexity. Its inferior limit corresponded to the plane 30 mm above the AC-PC plane.
For each subject in each VOI, we determined the clusters of significantly activated voxels on the z-score map for each task and calculated the mean location in Talairach coordinates for those voxels. We tested the significance of differences between the Talairach coordinates for pursuit- and saccade-related activation in each VOI with a t-test (2-sample assuming unequal variances) with a correction of degrees of freedom based on the original voxel size. We also determined the centroids of pursuit- and saccade-related activity as the grand mean (± SD) of the individual subject means of the Talairach coordinates for pursuit- and saccade-related activation.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
All subjects demonstrated both pursuit- and saccade-related activity in FEF, SEF, PEF, precuneus, and MT/MST, except for subject S4, who did not show any pursuit-related activity in the FEF and left PEF. In each cortical region, the activation during pursuit eye movements was smaller than during saccades in terms of spatial extent. Figure 2A indicates the mean Talairach coordinates across subjects for each region plotted on mean spatially normalized axial structural images of the five subjects. Figure 2B illustrates the spatial extents of significant activity across subjects calculated in each VOI for both eye movement tasks. Tables 1-5 show the Talairach coordinates of the mean location of pursuit- and saccade-related activity in the five anatomically defined VOIs. Figure 3 illustrates both pursuit- and saccade-related activity in all the cortical regions in one subject (S5).
|
|
|
|
|
|
|
Four of 5 subjects showed bilateral pursuit-related activity in the
FEF, and all subjects showed saccade-related activity. The centroid of
pursuit-related activity was inferior to the centroid of
saccade-related activity [Fig. 2A, right: mean
difference in 4 subjects = 4 mm; P < 0.05 in 2/4
subjects; the 2 remaining subjects (S1 and S2) showed the same trend,
but the difference of 2 mm did not reach statistical significance;
left: mean difference in 4 subjects = 3 mm,
P < 0.05 in 3/4 subjects; the remaining showed the
opposite difference, Table 1]. The pursuit-related centroid was also
significantly lateral to the saccade-related centroid in the right
hemisphere (Fig. 2A; mean difference in 4 subjects = 9 mm; P < 0.005 in 3/4 subjects; the remaining subject did not show any difference, Table 1). The same trend was observed in
the left hemisphere (Fig. 2A; mean difference in 4 subjects = 3 mm) but was statistically significant in only one
subject (S2; Table 1). The spatial extent of pursuit-related activity was significantly smaller than the spatial extent of saccade-related activity in the left hemisphere (Fig. 2B; 1.5 vs. 5.4 cm3, respectively, P = 0.03). The same
trend was observed in the right hemisphere but failed to reach the
statistical significance (Fig. 2B; 1.3 versus 4.9 cm3, respectively, P = 0.06). Note also
that the spatial extent in the right and left hemispheres was
equivalent for pursuit- (1.5 vs. 1.3 cm3, respectively) and
saccade-related activity (5.4 vs. 4.9 cm3, respectively).
These findings are consistent with our previous report based on the
same data in which we examined the Talairach coordinates of the maximum
of pursuit- and saccade-related activity in the FEF (Petit et
al. 1997a).
All subjects showed activation of the SEF during the two oculomotor tasks (Table 2). The centroid of pursuit-related activity was significantly posterior to the centroid of saccade-related activity (Fig. 2A; mean difference in 5 subjects = 8 mm; P < 0.05 in all cases, Table 2). The spatial extent of pursuit-related activity was significantly smaller than the spatial extent of saccade-related activity (Fig. 2B; 0.7 vs. 4.3 cm3, respectively, P = 0.03).
All subjects showed bilateral activation of the PEF, except one subject (S4), who did not show any pursuit-related activity in the left IPS. The centroid of pursuit-related activity tended to be posterior to the centroid of saccade-related activity in both hemispheres [Fig. 2A, right: mean difference in 5 subjects = 13 mm; P < 0.005 in 3/5 subjects; 1 subject (S1) showed the same trend, but the difference of 2 mm did not reach the statistical significance, and the remaining subject (S2) showed the opposite difference; left: mean difference in 4 subjects = 4 mm, P < 0.005 in 2/4 subjects; 1 subject (S1) showed the same trend, but the difference of 3 mm did not reach statistical significance, and the remaining subject (S3) showed the opposite trend, Table 3]. The spatial extent of pursuit-related activity was significantly smaller than the spatial extent of saccade-related activity in the right hemisphere (Fig. 2B; 1.2 vs. 7.5 cm3, respectively, P = 0.02). The same trend was observed in the left hemisphere but did not reach statistical significance (Fig. 2B; 2.0 vs. 4.5 cm3, respectively, P = 0.08)
All subjects showed activation of the precuneus during both pursuit and saccade tasks. As illustrated in Fig. 2A, the centroid of pursuit-related activity was significantly posterior and inferior to the centroid of saccade-related activity (mean difference for the y-coordinates in 5 subjects = 10 mm; P < 0.05 in all cases; mean difference for the z-coordinates in 5 subjects = 7 mm; P < 0.05 in 4/5 subjects, Table 4). Although the spatial extent of pursuit-related activity was smaller than the spatial extent of saccade-related activity, they did not differ significantly (Fig. 2B; 2.6 versus 4.5 cm3, respectively, P = 0.2).
All subjects showed bilateral activation of the occipitotemporal cortex during both pursuit and saccade tasks. The centroid of pursuit-related activity was significantly posterior to the centroid of saccade-related activity in most subjects [Fig. 2A, right: mean difference in 5 subjects = 8 mm; P < 0.05 in 4/5 subjects; the remaining subject (S2) showed no difference; left: mean difference in 5 subjects = 6 mm, P < 0.05 in 4/5 subjects; the remaining subject (S5) showed the same trend, but the difference of 3 mm did not reach statistical significance, Table 5]. The spatial extents of both pursuit- and saccade-related activity did not differ significantly (left: 2.0 vs. 2.6 cm3, right: 3.2 vs. 4.9 cm3, respectively, P = 0.2; Fig. 2B).
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The performance of pursuit eye movements induced activations in a set of cortical regions known to subserve the control of saccadic eye movements, namely the FEF, SEF, PEF, precuneus, and MT/MST. In addition, the current findings provide the first functional imaging evidence for a distinction between the functional anatomy of the two cortical networks subserving pursuit and saccadic eye movements.
FEF
Execution of both pursuit and saccadic eye movements induced
bilateral activation located in the precentral gyrus. This anatomic location corresponds to the human FEF as previously identified (for
review see Luna et al. 1998; Paus 1996
;
Petit et al. 1996
). Further, the mean locations of
pursuit-related activity were most often inferior to the mean locations
of saccade-related activity and also tended to be more lateral. This
result was included in our preliminary report on this study but with a
different measure of location, namely peak activity (Petit et
al. 1997a
). The current findings thus provide evidence for two
different subregions in the human FEF related to the execution of
smooth pursuit and saccadic eye movements. Aside from our preliminary
report, previous pursuit-related FEF activation in healthy humans has
been reported only in abstract form (Berman et al. 1996
;
Brandt et al. 1997
; Colby and Zeffiro 1990
; Sweeney et al. 1998
). Clinical studies
have also recently described an impairment of smooth pursuit eye
movements related to lesions that encompassed both precentral and
posterior part of superior and middle frontal gyrus (Heide et
al. 1996
; Lekwuwa and Barnes 1996
; Morrow
and Sharpe 1995
; Rivaud et al. 1994
).
In monkeys, both single-cell recording and intracortical
microstimulation have shown that the monkey FEF also contributes to the
control of smooth pursuit (Gottlieb et al. 1994;
Tian and Lynch 1996a
,b
). The pursuit-related area
encompasses a small part of the monkey FEF territory, posterior to the
dominant saccade-related area. This study also identified a smaller
pursuit-related subregion in human FEF compared with the
saccade-related FEF, which parallels results observed in the monkey.
SEF
Both pursuit- and saccade-related activity were observed in the
SEF in each subject. The mean location of the saccade-related SEF
activation in this study was similar to the location of medial superior
frontal activation previously observed during the execution of
different types of saccadic eye movements, PET (Anderson et al.
1994; Dejardin et al. 1998
; Fox et al.
1985
; Lang et al. 1994
; O'Sullivan et
al. 1995
; Paus et al. 1993
; Petit et al.
1993
, 1996
; Sweeney et al. 1996
) and fMRI
(Darby et al. 1996
; Luna et al. 1998
).
This study provided the first functional imaging evidence of a specific
SEF activation during smooth pursuit eye movements, in the posterior
part of the SEF. A similar distinction has also been reported recently
in abstract form (Sweeney et al. 1998
). A role for the
SEF in pursuit eye movements has also been documented recently in the
clinical literature (Heide et al. 1996
; Lekwuwa and Barnes 1996
; Morrow and Sharpe 1995
).
In monkeys, the SEF was first defined as an area involved in saccadic
eye movements (for review see Tanji and Shima 1996; Tehovnik 1995
). Pursuit-related neurons were found in
the monkey SEF (Heinen 1995
; Schall 1991
;
Schlag et al. 1992
), and smooth eye movements have been
reliably evoked by microstimulation at low threshold (Tian and
Lynch 1995
, 1996a
). To our knowledge, no topological
relationship has been described between the pursuit- and
saccade-related subregions in the monkey SEF. Most of the monkey SEF
territory is concerned with saccadic eye movements, whereas only a
single relatively small zone is responsible for pursuit eye movements.
It is noteworthy that this study also identified a smaller
pursuit-related area in human SEF than the saccade-related SEF, which
parallels and extends results previously observed in the monkey.
PEF
Performing visually guided pursuit and saccadic eye movements induced distinct bilateral activation within the IPS, extending onto the gyral surfaces of both the inferior and superior parietal lobules, which identified the location of the PEF in each subject. To our knowledge, pursuit-related activity within the intraparietal sulcus has never been reported.
The mean location of the saccade-related PEF activation in this study
was similar to the location of intraparietal activation previously
observed during the execution of different type of saccadic eye
movements, PET (Anderson et al. 1994; Kawashima
et al. 1996
; O'Sullivan et al. 1995
;
Paus et al. 1993
; Petit et al. 1996
;
Sweeney et al. 1996
) and fMRI (Darby et al.
1996
; Luna et al. 1998
; Müri et al.
1996
). In patients, lesions overlapping IPS, in the superior
part of the angular gyrus and supramarginal gyrus (area 39 and 40 of
Brodmann), resulted in increased latency of visually guided saccades
(for review see Pierrot-Deseilligny 1994
, 1995
). A
recent clinical study also described an impairment of smooth pursuit
eye movements related to lesions that encompassed the angular and
supramarginal gyri and the adjacent occipitotemporal cortex
(Heide et al. 1996
).
In monkeys, it is well established that the PEF participates in both
pursuit and saccadic eye movements (for review see Andersen and
Gnadt 1989; Bremmer et al. 1997a
; Colby
et al. 1993
; Lynch et al. 1977
;
Mountcastle et al. 1975
; Sakata et al.
1983
; Tian and Lynch 1996b
). Tian and Lynch have
recently demonstrated that there are two distinct groups of neurons
labeled by injections in the pursuit- and saccade-related monkey FEF
(Tian and Lynch 1996b
). One group of PEF neurons,
labeled by the pursuit-related FEF injection, is located dorsally and
posteriorly to another group of PEF neurons labeled by the
saccade-related FEF. It is noteworthy that this study also identified a
pursuit-related area in human PEF that is posterior to the
saccade-related PEF (Fig. 2).
MT/MST
Both pursuit- and saccade-related activations were observed
bilaterally in the lateral occipitotemporal cortex along and at the
junction of the ascending limb of the inferior temporal cortex and the
lateral occipital sulcus, which is thought to be the human homologue of
motion-sensitive MT/MST in the monkey and has also been called area V5
(Watson et al. 1993; Zeki et al. 1991
).
Although the location of the present MT/MST activation was not
corroborated with a separate study at the response to visual motion
without eye movements, its anatomic location and Talairach coordinates indicate that it corresponds to the motion-sensitive MT/MST
(Corbetta et al. 1990
; Tootell et al.
1995
; Watson et al. 1993
; Zeki et al.
1991
). Our results provide the first evidence that MT/MST showed differential activity during the execution of smooth pursuit and
saccadic eye movements.
A previous fMRI study showed that the lateral occipitotemporal cortex
was more activated during smooth pursuit eye movement than during
observation of a moving grating with the eyes still (Barton et
al. 1996; see also in abstract form Brandt et al. 1997
, 1998
). Until now, however, visually guided saccade-related
activity in the lateral occipitotemporal cortex has never been
reported. A focal activation at the junction of parietal, temporal, and occipital cortex has only been reported recently during the execution of memory-guided saccades (Sweeney et al. 1998
). Smooth
pursuit deficits have been documented in the clinical literature
(Heide et al. 1996
; Lekwuwa and Barnes
1996
; Pierrot-Deseilligny 1994
), but no specific
deficit during the generation of visually guided saccades has been
described after occipitotemporal lesions (but see Heide et al.
1996
). The extent to which the current saccade-related activity
is only a response to moving targets and/or is related to extraretinal
inputs such as eye movement signal during saccade cannot be resolved on
the basis of current results and requires further investigation.
In monkeys, cortical area MT appears to be highly specialized for the
analysis of visual motion (Komatsu and Wurtz 1988). Neural activity related to pursuit eye movements has been reported in
both MT and MST areas (Komatsu and Wurtz 1988
), and
lesions of either MT or MST impair ocular pursuit area of moving
targets (Dürsteler and Wurtz 1988
). As emphasized
recently (Tian and Lynch 1996b
), there have been almost
no studies that have investigated MT/MST areas in monkeys regarding
their role in saccadic eye movement control.
It has been argued that the impairments of pursuit eye movements after
MT/MST lesions could be due to degraded perception of the image motion
of a target on the retina. However, MST also receives input related to
eye movement during pursuit, but MT does not receive this extraretinal
input (Newsome et al. 1988). MST therefore appears to be
involved in the synthesis of the pursuit command, which requires
information about both the motion of the target on the retina and
current eye movement (Lisberger et al. 1987
). In their
fMRI study, Barton et al. (1996)
concluded that pursuit-related
activity in the lateral occipitotemporal cortex represented a
combination of residual motion signals and extraretinal inputs,
including both an attentional modulation and an eye movement signal
during pursuit (Barton et al. 1996
). The current
findings are consistent with this conclusion.
Precuneus
Both pursuit- and saccade-related activity was observed in the
precuneus in each subject. The mean location of the saccade-related precuneus activation was similar to the location of precuneus activation previously observed during the execution of saccadic eye
movements (Anderson et al. 1994; Darby et al.
1996
; Luna et al. 1998
; Petit et al.
1996
). The current study provided the first functional imaging
evidence of a specific precuneus activation during smooth pursuit eye
movements, posterior and inferior to the saccade-related precuneus
activation. To our knowledge, no specific oculomotor role has been
attributed to this medial cortical region.
In monkeys, a large area in the medial wall of the posterior parietal
lobe [area 7m and the dorsomedial visual area (DM)] appears to play a
role in oculomotor control (Cavada and Goldman-Rakic 1989a,b
; Tian and Lynch 1996b
). Both area 7m and
DM appear to be involved in the transmission of visual motion
information from the visual cortex to the FEF (Tian and Lynch
1996b
). Although the homologies between areas in the posterior
parietal cortex in monkeys and humans are still unclear, the current
findings may parallel the organization of the medial part of the
parietal cortex in monkeys.
Parallel corticocortical systems serving pursuit and saccadic eye movements
The current results support the hypothesis developed from monkey
studies that there are two parallel corticocortical systems devoted to
the control of purposeful eye movements (Tian and Lynch 1996b). One of these systems controls visual pursuit eye
movements, and the other controls visually guided saccadic eye
movements. Each system is composed of several interconnected subregions
distributed across different cortical eye fields such as the FEF, SEF,
PEF, MT/MST, and dorsomedial parietal visual areas. Within each
cortical eye field, one group of neurons serves as a subregion in the
network devoted to saccadic eye movements, and a second group,
generally non overlapping, serves as a subregion devoted to pursuit eye movements (see Fig. 11 of Tian and Lynch 1996b
).
The current fMRI study provides the first functional imaging evidence of such parallel corticocortical systems subserving pursuit and saccadic eye movements in healthy humans. Each network would be composed of the same cortical eye fields, namely the FEF, SEF, PEF, MT/MST, and precuneus, with different pursuit- and saccade-related subregions in each field. We observed some overlap between both pursuit and saccade-related subregions in each cortical eye field, which could be due to spatial resolution of fMRI. However, we have shown that pursuit-related areas could be distinguished from saccade-related areas in terms of both spatial extent and location.
![]() |
ACKNOWLEDGMENTS |
---|
We thank E. Hoffman, K. Keil, and J. Schouten for help with subject recruitment and scheduling; S. Courtney, J. Ingeholm, F. Lalonde, and V. Clark for assistance with eye movement and fMRI data acquisitions; and the staff of the National Institutes of Health in vivo nuclear magnetic resonance (MR) center for assistance with MR scanning.
This work was supported by the National Institute of Mental Health's Intramural Research Program. L. Petit was supported by the FYSSEN Foundation and Philippe Foundation.
![]() |
FOOTNOTES |
---|
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 20 May 1998; accepted in final form 3 February 1999.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|