Section of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06520-8001
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Russo, Gary S. and Charles J. Bruce. Supplementary Eye Field: Representation of Saccades and Relationship Between Neural Response Fields and Elicited Eye Movements. J. Neurophysiol. 84: 2605-2621, 2000. The functional organization of the low-threshold supplementary eye field (SEF) was studied by analyzing presaccadic activity, electrically elicited saccades, and the relationship between them. Response-field optimal vectors, defined as the visual field coordinates or saccadic eye-movement dimensions evoking the highest neural discharge, were quantitatively estimated for 160 SEF neurons by systematically varying peripheral target location relative to a central fixation point and then fitting the responses to Gaussian functions. Saccades were electrically elicited at 109 SEF sites by microstimulation (70 ms, 10-100 µA) during central fixation. The distribution of response fields and elicited saccades indicated a complete representation of all contralateral saccades in SEF. Elicited saccade polar directions ranged between 97 and 262° (data from left hemispheres were transformed to a right-hemisphere convention), and amplitudes ranged between 1.8 and 26.9°. Response-field optimal vectors (right hemisphere transformed) were nearly all contralateral as well; the directions of 115/119 visual response fields and 80/84 movement response fields ranged between 90 and 279°, and response-field eccentricities ranged between 5 and 50°. Response-field directions for the visual and movement activity of visuomovement neurons were strongly correlated (r = 0.95). When neural activity and elicited saccades obtained at exactly the same sites were compared, response fields were highly predictive of elicited saccade dimensions. Response-field direction was highly correlated with the direction of saccades elicited at the recording site (r = 0.92, n = 77). Similarly, response-field eccentricity predicted the size of subsequent electrically elicited saccades (r = 0.49, n = 60). However, elicited saccades were generally smaller than response-field eccentricities and consistently more horizontal when response fields were nearly vertical. The polar direction of response fields and elicited saccades remained constant perpendicular to the cortical surface, indicating a columnar organization of saccade direction. Saccade direction progressively shifted across SEF; however, these orderly shifts were more indicative of a hypercolumnar organization rather than a single global topography. No systematic organization for saccade amplitude was evident. We conclude that saccades are represented in SEF by congruent visual receptive fields, presaccadic movement fields, and efferent mappings. Thus SEF specifies saccade vectors as bursts of activity by local groups of neurons with appropriate projections to downstream oculomotor structures. In this respect, SEF is organized like the superior colliculus and the frontal eye field even though SEF lacks an overall global saccade topography. We contend that all specialized oculomotor functions of SEF must operate within the context of this fundamental organization.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Schlag and Schlag-Rey (1985,
1987
) initially defined the supplementary eye field (SEF) of
the macaque monkey as a discrete region of dorsomedial frontal cortex
where saccadic eye movements are electrically elicited with low
currents. SEF lies just anterior to the supplementary motor area (SMA)
from which skeletalmotor movements can be elicited (e.g.,
Woolsey et al. 1952
) and medial to the better known
frontal eye field (FEF) from which both saccades (e.g., Bruce et
al. 1985
; Robinson and Fuchs 1969
) and smooth pursuit (e.g., MacAvoy et al. 1991
) can be elicited.
Schlag and Schlag-Rey (1985, 1987
) also reported
that neurons in SEF responded to the appearance of visual stimuli and
in conjunction with saccadic eye movements. This basic result has been
confirmed by their subsequent studies (e.g., Schlag-Rey et al.
1997
) and in other laboratories, including ours (Russo
and Bruce 1996
; Schall 1991a
,b
). Moreover,
several interesting and complex aspects of SEF activity indicating
several possible specializations have since been examined (see
DISCUSSION). However, some basic response properties of SEF
neurons, and the functional relationship between the saccades
electrically elicited from SEF and the activity of SEF neurons, remain
unknown. This void exists, at least in part, because research has not
been restricted to the SEF but rather reflected recordings from a
larger zone of dorsomedial frontal cortex and has involved either no
microstimulation to confirm that recordings were from SEF or
stimulation with large currents that can elicit saccades from well
outside SEF. In addition, some basic functional issues were unresolved
because it was initially reported by Schlag and Schlag-Rey
(1987)
that the saccades electrically elicited from SEF were
not always "constant vector" in nature but rather often seemed
"goal-directed." They hypothesized that SEF served to move the eye
to particular orbital positions and thus to code saccades in a
craniocentric coordinate system. However, after systematically
investigating the orbital dependence of saccades electrically elicited
from the low-threshold SEF using arrays of fixation positions and
testing FEF using the same methods and subjects, we established that
saccades elicited from SEF are basically oculocentric with generally
modest orbital position effects that are very similar to what is found
in FEF (Bruce 1990
; Russo and Bruce
1993
). Furthermore we later demonstrated that SEF visual receptive fields are oculocentric, not craniocentric, and that SEF
movement fields are oculocentric as well (Russo and Bruce 1996
).
Although our conclusion that SEF codes saccades oculocentrically has not yet been unanimously accepted, we set out to further study, in an oculocentric framework, the basic neural mechanisms used by SEF to generate saccadic behavior. We mapped the response fields of SEF neurons, both visual receptive fields and saccadic movement fields, and measured the saccades evoked by activating those neurons and their immediate neighbors via electrical microstimulation. Both response-field mapping and electrical stimulation were performed while the monkeys fixated a centrally located fixation point, and both types of data were analyzed in terms of their polar direction and amplitude. A close correspondence between the neural response fields and the dimensions of elicited saccades would indicate a functional linkage between the discharge of a discrete set of SEF neurons and the generation of specific saccade metrics, whereas a lack of correspondence would suggest that SEF is functionally specialized for nonspatial or other more complex aspects of saccade programming. We also investigated the overall physiological organization of SEF by analyzing the saccade parameters encoded by adjacent neurons and stimulation sites (especially those recorded within the same electrode penetration or at the same cortical locus) and the mapping of saccade direction and amplitude across the tangential dimensions of SEF.
We found that neural activity in SEF during visually guided saccades is composed primarily of a visual component and a movement component and that the response fields of these two activities were strongly correlated with each other as well as with the saccades electrically elicited from the recording site. Thus the representation of visual stimulus location and saccade metrics were aligned. We also found similar representations of saccade direction along different cortical depths during the same electrode penetration, indicating a columnar organization. Although the total distribution of response fields and elicited saccades suggested that each SEF contains a complete representation of all possible saccades into the contralateral visual hemifield, saccades were not topographically organized across SEF in a simple way. Instead the representation of saccades was fairly patchy with hints of systematic shifts in direction more indicative of a hypercolumnar-type organization. We conclude that SEF participates in the transformation of visual stimulus location into saccadic commands via the punctuated activity of particular groups of SEF neurons that in turn project to downstream oculomotor structures in a topographic manner. In this regard, the basic sensorimotor mechanisms of SEF are similar to those of FEF and the superior colliculus. Thus any functional specializations of SEF must operate within the context of this core neurophysiological framework.
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Surgical and behavioral protocols were approved by the Institutional Animal Care and Use Committee and complied with United States Public Health Service policy on the humane care and use of laboratory animals.
Single-neuron recording
Three female rhesus monkeys (Macaca mulatta) were
prepared for chronic single-neuron recording in three separate aseptic
surgical procedures. These three monkeys were the same monkeys used in two previous SEF studies (Russo and Bruce 1993, 1996
).
During experimental sessions, each monkey sat in a primate chair with its head held stationary by a restraining receptacle fixed to the
skull. Eye-position coordinates were obtained with a search coil
implanted in one eye (Judge et al. 1980
). Neurons were
recorded with microelectrodes made from either glass-coated Elgiloy
wire (tip exposures, 30-50 µm) or glass-coated platinum/iridium wire (tip exposures, 10-30 µm), which were advanced through the intact dura with a hydraulic microdrive (MO-95, Narishige) mounted on recording chambers. The minimum penetration spacing across the cortical
surface was 0.5 mm. However, in cases where multiple penetrations were
made at the same microdrive coordinate, the slight curvature of the
electrode was used to vary the cortical tissue sampled by rotating the
electrode in the microdrive ~90° between experimental sessions.
Time-amplitude window discriminators (DIS-1, BAK Electronics) sorted
action potentials for sampling by the computer.
Behavioral methods
Visual stimuli were small white spots presented on a 27-in color
monitor (CS-2669R, Mitsubishi) located 47 cm from the monkey's eyes
and subtending 66 by 44° of visual angle. Four tasks were used to
analyze presaccadic activity and map response fields. In all four
tasks, each trial began when the monkey achieved and maintained
fixation of a solitary spot for 0.5 s. At the end of each correctly
performed trial, all remaining visual stimuli were extinguished and the
monkey was rewarded with ~0.2-ml of dilute fruit drink.
VISUAL-SACCADE TASK. The appearance of a peripheral visual stimulus coincided with the disappearance of the original fixation target, and the monkey was required to saccade directly to the new target. This task was the simplest way to determine if neurons had saccade-related activity, and an interactive version, wherein the experimenter used a joystick to re-position the peripheral target location between trials, was often the first task used to test each neuron.
VISUAL-PROBE TASK. A visual stimulus was presented in the periphery, but in this task, the fixation target remained on and the monkey was rewarded for simply continuing to fixate it. Conversely the trial was terminated if the monkey incorrectly made a saccade away from the original fixation target. This task was used to map neurons with purely visual responses.
DEFERRED-SACCADE TASK. Shortly after the monkey foveated the fixation target, a peripheral target was presented while the fixation target remained on. The monkey was required to saccade to this second target but only after the original fixation target disappeared, usually 0.5-1.0 s after the peripheral target's appearance. By temporally separating the appearance of the peripheral target from the signal to saccade to it, this task dissociated activity related to the initial presentation of the visual stimulus from activity related to the execution of the saccadic eye movement even though the saccade was visually guided.
MEMORY-SACCADE TASK. The monkey was presented with a brief (0.5 s) visual target in the periphery while foveating a continuously illuminated fixation target. After 0.5-1.0 s, the fixation target disappeared, signaling the monkey to saccade to the location where the peripheral target had previously appeared. This task best dissociated visual activity from movement activity because, in addition to temporally separating the presentation of the stimulus and the execution of the saccade, there was no overt target present when the saccade was made.
The memory-saccade task, performed in complete darkness, was used whenever possible to classify each neuron's presaccadic activity as having visual, movement, or both visual and movement components (see Bruce and Goldberg 1985Microstimulation
After studying a neuron, we tested for electrically elicited
saccades by stimulating through the recording microelectrode before
advancing it. The stimulation parameters used were the same or similar
to the stimulation parameters used in other studies of FEF and SEF.
Stimulation consisted of 70-ms trains of 350-Hz biphasic
(negative-positive) shocks (thus ~24 shocks per train) with duration
of 0.2 ms per phase. Stimulation was applied during fixation of a
target at or near the center of the screen, and the threshold of a
cortical site was defined as the magnitude of negative-going current
necessary to elicit saccadic eye movements on ~50% of trials.
Threshold estimation during fixation is quite conservative relative to
thresholds measured outside a formal task because attentive fixation
raises the threshold for electrically eliciting saccadic eye movements
from the FEF (Goldberg et al. 1986) and elsewhere.
Although we sought recording sites with low (50 µA) thresholds, sites
with slightly higher thresholds (
100 µA) were included in our final
analysis if robust presaccadic activity was recorded there and low
thresholds for eliciting saccades were eventually obtained, either in
the same penetration when the electrode tip was advanced into the
deeper cortical layers or in other penetrations at the same coordinates
or coordinates not more than 1 mm distant. Sites requiring currents
100 µA to obtain elicited saccades were not included in our
population summaries even if they were located within the SEF as
determined by the cortical boundary defined by the set of low-threshold sites.
Data analysis
Neural discharge rates were computed by estimating the onset and offset of the averaged response using the inflection points of cumulative histograms aligned to either cue onset (visual activity) or saccade beginning (movement activity) and then extracting the trial-by-trial spike rates during this period. The start and end of elicited saccades were found by the computer using an algorithm based on eye velocity.
The optimal polar direction of neural activity was estimated using an
array of visual cues all having the same eccentricity but
systematically varying in polar direction. The spike rates for each cue
direction were fit to the Gaussian function
![]() |
The angular-angular correlation (raa)
between the optimal direction of neural activity
(v or
m) and the
median elicited saccade direction obtained at the neuron's site
(
e) were computed using the formula of Fisher
and Lee (Fisher 1993
, p. 151). For all statistics and
plots, polar directions obtained from left cerebral hemispheres were
transformed into a right-hemisphere convention by the formula
' = 180 -
so that all contralateral directions lie between 90 and
270° regardless of hemisphere.
Optimal eccentricity (i.e., polar amplitude, radius, or distance) of
neural activity was estimated using an array of visual cues all having
the same polar direction but systematically varying in eccentricity.
These data were fit to the Gaussian function
![]() |
For some neurons, the formal testing of optimal direction or
eccentricity with uniformly spaced arrays of visual cues could not be
completed (usually because the neuron was lost or the monkey stopped
working before the neuron could be formally tested). In some of these
cases, we successfully estimated their optimal direction and
eccentricity by fitting the neural activity recorded during our
preliminary test that used an interactive joystick to re-position the
visual cue between trials. We fit these data to the general Gaussian
function of direction and eccentricity
![]() |
For the purpose of analyzing the uniformity of a set of directions
represented at nearby SEF sites, the mean vector length r
(Batschelet 1985, p. 10) was used as an index of
"directional-concentration," the formula being
![]() |
Histology
At selected recording sites, electrolytic lesions were made by passing 20 µA of negative current through the electrode for 30 s. Other sites were marked with iron by passing 10 µA of positive current through Elgiloy electrodes for 3 min.
Monkeys AB and SY were deeply anesthetized with pentobarbital sodium and perfused transcardially with saline, followed by 10% formalin in 0.1 M phosphate buffer and a sucrose series. Monkey HK died unexpectedly and could not be perfused. Instead, its brain was fixed by immersion for 7 days in a mixture of 1.25% glutaraldehyde and 1% paraformaldehyde in 0.1 M phosphate buffer followed by 3 days in the same fixative with 30% sucrose. All brains were photographed, blocked in the coronal plane, and sectioned at 50 µm on a freezing microtome. Every other section through the region with electrode penetrations were reacted with ferrocyanide (Perl's reaction) for visibility of the iron deposits and counter stained with neutral red. Individual recording and stimulation sites that had been marked with deposits or lesions were identified.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Location of low-threshold SEF
Both hemispheres of two monkeys (AB and SY)
and one hemisphere of one monkey (HK) were studied. For each
of these five hemispheres, the low-threshold SEF was defined as the
contiguous cortical area whose boundary was not more than 1 mm from an
electrode penetration coordinate containing at least one site with a
low (50 µA) threshold for eliciting saccadic eye movements. Using
this criteria, the low-threshold SEF was typically found to be located
in a small region (10-15 mm2) on the dorsomedial
convexity of the frontal lobe with its center ~5 mm anterior to the
most posterior level of the arcuate sulcus and 2-3 mm lateral to the
lip of the longitudinal fissure. Figure 1
shows the location of electrode penetrations in the right hemisphere of
monkey AB using different symbols to denote the lowest
threshold found at each penetration coordinate. An example of one
electrically elicited saccade from one low-threshold SEF site is also
shown along with its histological confirmation. We rarely saw evoked movements other than saccades in the low-threshold SEF; the only exceptions were four electrode penetrations where both evoked saccades
and pinna movements were observed. Most electrically elicited pinna
movements were evoked at sites posterior and lateral to SEF, whereas
skeletal movements were evoked several millimeters posterior to SEF. We
did not see any elicited smooth eye movements, such as are elicited
from the depths of the arcuate sulcus (MacAvoy et al.
1991
).
|
The low-threshold saccadic SEF is the subject of this report. Our study is based on elicited saccades from 109 stimulation sites and 160 presaccadic neurons, all located within the low threshold SEF as defined in the preceding text. We first present summaries of the stimulation and neural activity data separately, then present data showing how they are related to each other, and finally show how they are organized across SEF.
Electrically elicited saccades
Figure 2 summarizes our elicited-saccade database pooled across the five hemispheres we studied. Saccades were electrically elicited during attentive fixation of a small spot at the center of the monitor (see METHODS). Thresholds ranged from 10-90 µA (Fig. 2, top left), with a median threshold of 40 µA. Elicited saccade data from stimulation sites with thresholds >50 µA but <100 µA were included in our analyses if they were located within the boundary of low-threshold SEF sites. Neurons at these slightly higher threshold sites usually exhibited robust presaccadic activity similar to that found at low-threshold sites. We would expect that these thresholds would be significantly lower if stimulation had been tested while the monkey alertly looked about without any overt fixation targets; however, we did little testing of this type.
|
The median cortical depth of the 109 stimulation sites was 1.85 mm below the apparent start of neural activity. Only 7 of the 109 sites was at a depth <0.8 mm as we did not find low thresholds (or robust presaccadic activity) until ~1 mm or more below the apparent entry of the electrode into the cortex.
Because threshold currents elicited saccades on only ~50% of trials, we usually increased the current ~10 µA after determining each site's threshold to quickly obtain representative sets of elicited saccades at fixed currents. These testing currents ranged from 15 to 100 µA, with a median of 50 µA (Fig. 2, middle left).
The latency of electrically elicited saccades, defined as the time from
the start of the stimulation train to the start of the saccadic
movement, was generally very short (Fig. 2, bottom left).
The median latency was 50 ms, with 88% of the stimulation sites having
a median latency between 36 and 60 ms. However, the upper tail of the
latency distribution is long, and for eight sites, the elicited saccade
latency was even greater than the duration of the stimulation train
that we used (70 ms). We carefully examined the velocity profiles of
elicited saccades and found no indication that elicited saccades with
longer latencies were different from elicited saccades with shorter
latencies. In particular, they were not prematurely abbreviated by the
cessation of 70-ms stimulation train, even when the train ended before
the saccade began. Instead, all the saccades electrically elicited from
SEF exhibited the classic all-or-none ballistic features originally described for saccades elicited from FEF by Robinson and Fuchs (1969) with consistent amplitudes and directions regardless of latency.
We term the median elicited saccade, taken during central fixation, the characteristic saccade vector for a site. The distribution of characteristic saccade vectors from all 109 sites is shown in Fig. 2, right. For this and subsequent figures, characteristic saccades from left hemispheres are converted to a right-hemisphere convention by mirror reversing them as described in METHODS. For example, elicited saccades with a polar direction of 45° (upward and rightward) obtained from a left-hemisphere site would be converted to 135° (upward and leftward).
All 109 characteristic saccades were contralaterally directed. Their
directions (e) ranged from nearly straight up
(minimum 97°) to nearly straight down (maximum 262°), and nearly
all directions into the contralateral hemifield seem to be represented.
However, almost twice as many saccades were elicited into the upper
contralateral quadrant (65%) as into the lower quadrant (35%).
Characteristic elicited saccade amplitudes (
e)
ranged from small (1.8°) to large (26.9°), with a median of
13.1°.
Presaccadic response fields
We searched for neurons with presaccadic responses while the monkey performed either the visual-saccade or the deferred-saccade task (see METHODS) with the experimenter interactively varying the coordinates of the peripheral visual cue between trials with a joystick. When a SEF neuron with presaccadic activity was isolated, we first performed a set of preliminary tests to estimate the spatial location of the response field and classify its presaccadic activity as visual, movement, or visuomovement. An example of this preliminary testing procedure is illustrated in Fig. 3, A and B. Because a neuron's response field could be located at any point in the visual field, we first attempted to make a rough estimation of its location using the interactive version of the deferred-saccade task while watching the on-line raster display and listening to audio feedback of the neural response. The response field center of this neuron appeared to be directly downward (~270°) and ~10° eccentric. A retrospective quantitative analysis of these data confirmed that our initial estimate was fairly accurate (Fig. 3A, right). The three-dimensional plot shows the target coordinates of the 25 trials from this interactive task plotted along the x and y axes versus the neural response plotted along the z axis. The surface shows the best fit of these data to the Gaussian function for direction and eccentricity described in METHODS. The peak of the function was 263° in polar direction and 8.1° in eccentricity, fairly close to our on-line estimate of 270° in polar direction and 10° in eccentricity.
|
After approximating a neuron's response-field location, we analyzed the composition of its presaccadic activity using the memory-saccade task with a visual cue located at our initial on-line estimate (Fig. 3B). This neuron was classified as having visuomovement activity because it discharged in conjunction with the appearance of the peripheral visual cue and then again in conjunction with the saccadic eye movement.
Next we attempted to formally analyzed the spatial location of a
neuron's response field by determining its optimal direction and
optimal eccentricity in separate experiments Response-field direction
was analyzed by systematically varying the polar direction of the
visual cue around our initial on-line estimate while holding eccentricity constant, and response-field eccentricity was analyzed by
systematically varying the eccentricity of the visual cue around our
initial on-line estimate while holding direction constant. Figure 3,
C and D, shows this procedure for response-field
direction. Because this neuron exhibited both visual and movement
activities in the memory-saccade task (Fig. 3B), the
deferred-saccade task was used so that visual and movement activity
could be analyzed separately. These data were fit to the Gaussian
function described in METHODS to obtain independent
estimates of the neuron's visual activity optimal polar direction
(v) and movement activity optimal polar
direction (
m). Notice that the resulting
estimate of
v (258°) is very close to the
estimate of 263° obtained by fitting the informal, interactive data
described in Fig. 3A. However, the formal testing procedure
yielded a smaller SE for the
v estimate. Furthermore this neuron's
m could not be
accurately estimated with this set of interactive data even though it
was well estimated with the formal data. Thus the response-field
parameters estimated with our formal tests were generally more
accurate; however, some neurons mapped only informally were included in
our analysis if the data provided good fits yielding a
v and/or
m that
agreed with the on-line estimates.
A total of 160 presaccadic neurons in the low-threshold SEF were
successfully classified and mapped. The Venn diagram in Fig. 4 summarizes their response
classification: overall, 84% of these neurons had visual activity and
57% had movement activity. There were 68 (43%) with purely visual
responses, 26 (16%) with purely movement responses, and 66 (41%) with
both visual and movement responses. The median cortical depths for the
three neuronal types were 1.75 mm (visual), 2.18 mm (movement), and
1.68 mm (visuomovement). The null hypothesis of equality of depth
across neuron types is unlikely (Kruskal-Wallis
2[2] = 7.39, P < 0.025).
|
To illustrate the overall presaccadic responses of SEF, the average response histograms for 104 neurons tested on the memory saccade task are shown in Fig. 4, top (56 of the 160 neurons could not be tested on the memory saccade task because the monkey stopped working or the neuron was lost; they were classified on the basis of activity during the deferred-saccade task). These composite histograms were compiled by first computing histograms of neural activity for each neuron using target locations at or near the optimal location for their presaccadic responses, and then averaging them together. The activity of these 104 neurons aligned to cue onset, fixation offset, and saccade, beginning show that presaccadic activity in SEF is composed of two main components: a burst of activity in response to the appearance of a visual stimulus and a burst of activity preceding and during the saccade. Some tonic mnemonic activity is also evident, indicated by the small but significant elevation in tonic activity (~3 spikes/s) while fixating during the delay period, compared with the period of fixation before the peripheral cue was presented. A very similar pattern of activity was observed when these same neurons were tested with the deferred-saccade task. In general both the deferred-saccade task and the memory-saccade task gave similar results.
When the visual and movement activities of SEF visuomovement neurons
were mapped, their response fields were usually closely aligned. Of the
66 visuomovement neurons in our sample, we obtained quantitative
estimates of both v and
m for 44 of them. Figure 5 shows the relationship between
v and
m in these 44 neurons. Both visual and movement activity data were obtained from the same trials during the deferred-saccade or memory-saccade task. However, all estimates of
v and
m were from independent fits of distinct and
completely nonoverlapping visual and saccadic bursts. Although some
visuomovement neurons exhibited significant differences between
v and
m (the largest
was 57°), the median absolute difference was only 8° and with an
extremely strong correlation of 0.95. A linear regression of
m on
v yielded a
slope not significantly different from 1 (1.1 [0.94, 1.17]), and a
y intercept not significantly different from 0 (
14 [
35,
8]), indicating that the visual and movement fields of SEF
visuomovement neurons largely overlapped. This congruence of visual and
movement response fields is not only a principal finding but also
justifies using the mean of
v and
m as an estimate of a visuomovement neuron's
overall optimal direction (
vm) as described in
the following text.
|
Figure 6 shows the optimal response-field
vectors for all 160 SEF neurons considered in this report. The
direction of each neuron's response field was based on its estimated
v,
m, or
vm. The eccentricity of most response fields
were based on their optimal stimulus eccentricity
(
v) or optimal saccade amplitude (
m) obtained using the log-Gaussian fits
described in METHODS (and detailed in the following text)
or their mean if both were computed (
vm).
However, satisfactory estimates of
could not be computed for 50 of
the 160 neurons using either the formal or interactive tests. For these
50 neurons, we used our initial on-line estimate of response-field
eccentricity for the plots in Fig. 6; however, these data were not
included in further analyses of
(e.g., Fig. 11). As with the
electrically elicited saccades, the optimal response-field vectors of
left-hemisphere neurons were transformed into a right-hemisphere
convention. Compilation of all single-neuron data in this way provides
a comprehensive sample of the neural representation of saccades in SEF.
Notice that this collection of 160 optimal saccade vectors encompasses virtually all possible contralateral saccades, similar to the analogous
plot of elicited saccade vectors (Fig. 2). Unlike the elicited saccades
which were all contralateral, however, a few SEF neurons (5%, 8 of the
160) had unequivocally ipsilateral response fields. Another difference
between the response fields and the elicited saccades is that the upper
and lower contralateral quadrants were equally represented by visual,
movement, and visuomovement activity.
|
Relationship of presaccadic activity optimal direction to electrically elicited saccade direction
After mapping the presaccadic response field of a neuron, we
usually tested for electrically elicited saccades by stimulating through the recording electrode before moving it. Across all SEF sites
where both single neurons were mapped and saccades were elicited with
currents 100 µA, the neural response fields were highly predictive
of the elicited saccade dimensions. Figure
7A shows the analysis of
optimal direction for one SEF neuron that exhibited only visual
activity and the saccades subsequently elicited with electrical
stimulation at the neuron's recording site. The Gaussian fit indicated
a quite horizontal
v (183° ± 4°). After recording the activity of this neuron, and without moving the microelectrode, we electrically stimulated through the recording electrode. The 50% threshold for eliciting saccades at this site during central fixation was 20 µA, and the set of 10 elicited saccades shown in Fig. 7A, bottom, were obtained using 25 µA. The median elicited saccade direction
(
e) was 185°, very similar to the
v recorded at this stimulation site.
|
Figure 7B illustrates a similar analysis for a neuron with
presaccadic movement activity and no visual response. This neuron was
tested with the memory-saccade task using an array of eight visual cue
directions. The optimal saccade direction for the neuron's movement
activity was 119°. The saccades subsequently elicited by stimulation
using 30 µA had a median direction of 126°. Notice how
e is very close to
m.
Also notice that the elicited saccades are slightly more horizontal
than the neuron's optimal direction.
Figure 8 summarizes the relationship
between the response-field optimal direction of 77 SEF neurons and
electrically elicited saccade direction. As in Fig. 6, a single
neuron's optimal direction was derived from estimates of
v,
m, or
vm. The correlation between neural activity
optimal direction and elicited saccade direction was highly significant
(raa = 0.92). A separate analysis of
visual and movement activity (using estimates of
v from visual and visuomovement neurons and
estimates of
m from visuomovement and movement
neurons) yielded similarly strong correlations (visual activity:
raa = 0.94, n = 59;
movement activity: raa = 0.88, n = 42).
|
Although SEF neural activity and elicited saccade directions were
highly correlated, the precision of their alignment was not uniform
across the visual hemifield. In fact, the median absolute difference
for the 77 neurons in Fig. 8 was nearly 17°. Although some of this
discrepancy could be due to errors of measurement (our estimates of
v and
m typically had
an SE <10°), there was a conspicuous trend for sites with neurons
that had response fields nearly upward and downward to yield elicited
saccades that were slightly more horizontal. This trend was confirmed
by computing the linear regression of elicited saccade direction on
response-field direction. The slope of the regression line was 0.79 [0.71, 0.87], significantly less than unity inasmuch as its 95%
confidence interval does not include 1. Furthermore the complete
regression equation predicts that sites where neurons have response
fields directly up (90°) will yield elicited saccades that are 107°
in polar direction, and sites where neurons have response fields
directly down (270°) will yield elicited saccades that are 248° in
polar direction. Thus neurons at sites representing vertical directions
should yield elicited saccades rotated toward the horizontal an average of ~20°. An example of this phenomenon is shown in Fig.
9. This neuron's
v and
m was nearly
straight down (258 and 261°, respectively); however, the median
elicited saccade direction was 233°, thus rotated ~27°
contralateral from the neuron's response field.
|
Relationship of presaccadic activity optimal eccentricity to electrically elicited saccade size
Similar to the relationship between the optimal direction of
neural activity and the direction of saccades electrically elicited from the recording site, we found a relationship between a neuron's optimal eccentricity and the amplitude of subsequent electrically elicited saccades. However, this relationship was less precise than
what we found for polar direction. Figure
10 shows the neural recording and
electrical stimulation at three different SEF sites. The visual neuron
in Fig. 10, left, preferred moderate visual cue eccentricities (v = 12.4 ± 1.0°), and
medium-sized saccades were subsequently elicited
(
e = 8.5 ± 1.0°). The visual neuron in Fig. 10, middle, preferred large eccentricities
(
v = 29.6 ± 1.1°), and fairly large
elicited saccades were subsequently elicited (
e = 17.1 ± 0.7°). The movement neuron
in Fig. 10, right, clearly preferred very large saccades but
had very poor tuning for saccade size (
m = 47.5 ± 11.3°), and the subsequent elicited saccades were very
large (
e = 25.9 ± 2.5°). Figure
11 shows the optimal eccentricity of 60 neurons plotted against the median saccade amplitudes electrically
elicited from their recording sites. The correlation coefficient
(r = 0.49) is highly significant, but only about half
the correlation that was observed for the analysis of response field
versus elicited saccade direction. As in the analysis of saccade
direction, similar results were obtained when visual and movement
activity were considered separately.
v
obtained from visual and visuomovement neurons were significantly
correlated with
e (r = 0.48, P < 0.005, n = 44), as were
m and
e obtained from
visuomovement and movement neurons (r = 0.39, P < 0.05, n = 26).
|
|
Notice that most of the data points in Fig. 11 were below the
x = y diagonal, indicating that estimates of
optimal eccentricity were generally larger than elicited saccade
amplitude. One reason is that many SEF response fields were open ended
with responses that fell off very gradually, if at all, with increasing
eccentricity. As a result, the estimates v and
m for these eccentric response fields
generally had a correspondingly larger SE (see Fig. 10), making it
difficult to obtain a single accurate estimate of response-field optimal eccentricity that could be considered truly "optimal." Similar observations of open response fields have been made in the
superior colliculus (Munoz and Wurtz 1995
) and the FEF
(Bruce and Goldberg 1985
). Like
v and
m of
visuomovement neurons,
v and
m were also highly correlated
(r = 0.84, P < 0.005, n = 15). Such a small sample of visuomovement neurons
with both
v and
m
estimated again reflects the difficulty in estimating the optimal response-field eccentricity of SEF presaccadic activity.
Relationship of presaccadic activity type to electrically elicited saccade threshold
We compared the likelihood and ease of obtaining elicited saccades
at the sites of purely visual neurons, visuomovement neurons, and
movement neurons. Low-thresholds are more likely where FEF neurons have
movement activity (Bruce et al. 1985); however, we were
surprised to find that microstimulation was uniformly effective in
eliciting saccades at SEF sites, regardless of the type of presaccadic
activity there. Of the 68 SEF sites where visual neurons were recorded,
51 were tested with electrical stimulation. Of these tests, 82%
(42/51) elicited saccades, and the median threshold (regarding
threshold at the 9 unexcitable sites as large) was 52.5 µA. Of the 66 SEF sites where visuomovement neurons were recorded, 53 were tested
with electrical stimulation and 85% (45/53) elicited saccades with a
median threshold of 55 µA. Of the 26 SEF sites where movement neurons
were recorded, 21 were tested with electrical stimulation and 86%
(18/21) elicited saccades with a median threshold of 52.5 µA. A
2 test failed to indicate that these
percentages of elicited saccades differ significantly across neuron
types (
2[2] = 0.0239, P > 0.5), and a Kruskal-Wallis test failed to indicate that
thresholds differ across neuron types
(
2[2] = 0.7575, P > 0.5).
Topographic organization
The representation of saccades in SC has long been known to
have a straightforward topography, with small saccades represented anterior, large saccades posterior, upward saccades medial, and downward saccades lateral (Robinson 1972). In FEF
saccade amplitude is also topographically organized with large saccades
represented dorsomedially and small saccades ventrolaterally, but the
representation of saccade direction is more complex with gradual
changes in saccade direction as an electrode is advanced parallel to
the cortical surface resembling a hypercolumnar organization
(Bruce et al. 1985
). To determine what type of saccade
topography, if any, the low-threshold SEF has, we analyzed neural
response-field vectors and electrically elicited saccade dimensions
with respect to the relative location of the electrode tip within the
cortex. Although we did not find a systematic global topographic
organization of saccades across SEF, there was continuity of saccade
direction across short distances and evidence of columnar and
hypercolumnar organization with respect to polar direction.
As the electrode was advanced perpendicular to the cortical surface, neural response fields and elicited saccades represented similar saccade directions, indicating a columnar organization with respect to saccade direction. One example of this finding for neural activity is illustrated in Fig. 12, top left. In this electrode penetration, two superficially located neurons that were mapped simultaneously had response-field directions of 140 and 143°. Furthermore a neuron 0.45 mm deeper that was also mapped during the same experimental session had a response-field direction of 147°, very close to response-field direction of the two neurons recorded above them. Similar results were found when analyzing electrically elicited saccades. Figure 12, bottom left, shows the characteristic direction of saccades elicited from two different sites in the same electrode penetration. The characteristic elicited saccade direction from the more superficial stimulation site was 134° (threshold, 45 µA), and the characteristic elicited saccade direction from the stimulation site 1.3 mm deeper (threshold, 20 µA) was an almost identical 135°.
|
To examine columnar organization for all electrode penetrations with
more than one neuron or stimulation site, the mean vector length of
their characteristic directions was computed (see METHODS). Because the mean vector length indexes the concentration of directions around the circular mean, we call these measures
directional-concentration indexes (DCI). Indexes near 1 indicates a
very small deviation around the mean (and hence similar directions),
whereas smaller indexes indicate a larger deviation around the mean
(and hence diverse directions). The DCI of the penetration with three
neurons illustrated in Fig. 12, top left, was 0.998, consistent with their similar response-field directions. The DCI of the
penetration with two stimulation sites illustrated in Fig. 12,
bottom left, was 0.99996, consistent with their almost
identical characteristic directions. The histograms in Fig. 12,
right, show the distribution of DCIs for all penetrations
with multiple neurons and stimulation sites. The vast majority of DCIs
were between 0.95 and 1, with a median of 0.990 for response fields (37 electrode penetrations) and a median of 0.999 for elicited saccades (11 electrode penetrations). To check whether such large index values
simply reflected the strong contralateral bias of SEF, we used a
bootstrap technique to determine the distribution of DCIs expected by
chance. The median control DCIs computed from randomly shuffled data
(Fig. 12, -) were substantially smaller than most
experimental DCIs, and no control median (in 100 different control
shuffles) was as large as the experimental median (Fig. 12, - - -).
Thus the large number of indexes very close to 1 demonstrates that
different sites perpendicular to the cortical surface represent similar saccade directions, indicating that SEF has a columnar organization with respect to saccade direction.
To examine the topography of saccades across SEF tangential to the cortical surface., we computed a characteristic saccade vector for each electrode penetration (i.e., column) by taking the mean vector of all response fields and elicited saccades. Figure 13 shows these characteristic vectors for each of the five low-threshold SEF studied in this report. Visual inspection of these maps do not suggest a straightforward global topography of saccades across SEF. However, closer scrutiny reveals systematic shifts in saccade direction across patches of SEF. For example, the subset of coordinates in the right hemisphere of monkey AB enclosed in the gray box has characteristic directions that are directed predominantly downward in posterior penetrations and upward in anterior penetrations. This is more clearly demonstrated in Fig. 14, top, by plotting the surface coordinates along the x and y axes, and the penetration characteristic directions along the z axis. A planar regression was highly significant (r = 0.60, F[69,66] = 18.4, P < 0.0001), with the slope indicating a 55° change in polar direction per millimeter from the upper contralateral visual quadrant in anterior penetrations to the lower contralateral visual quadrant in posterior penetrations. Similar zones of systematic change in saccade direction along the anterior-posterior axis were also found in the left hemisphere of monkey AB and the right hemisphere of monkey HK. For all three hemispheres with significant regressions, the partial regression coefficients of saccade direction on anterior-posterior location were significant with 95% confidence, but the partial regression coefficients of saccade direction on medial-lateral location were not significant. No systematic change was evident in the left and right SEF of monkey SY, but these had the fewest electrode penetrations.
|
|
Although three hemispheres showed orderly progressions of saccade direction, their monotonic anterior-posterior pattern did not appear to describe a global SEF topography. Instead there were multiple horizontal saccade representations along the anterior and posterior extent of SEF in monkeys AB and HK (with unclear trends in SY), suggesting a hypercolumnar representation of saccade direction similar to what has been seen in the FEF with multiple representations of directions in a somewhat cyclical fashion. We illustrate this possibility in Fig. 14, bottom, by a least-squares fit of all the data from the right-hemisphere of monkey AB to a sinusoidal function. The fit is significant (F[69,66] = 1.715, P < 0.02) and appears to roughly model the change in direction along the anterior-posterior extent of SEF. Several incongruous points in this plot could reflect entry point inaccuracies in the microdrive/microelectrode system (see METHODS). Thus the conservative conclusion is that representation of saccade direction across the tangential extent of SEF is orderly but is not a straightforward global topography. Finally we did not find any systematic changes in saccade amplitude across SEF.
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Our previous work showed that SEF cortex encodes eye
movements in oculocentric coordinates, both in its response fields
(Russo and Bruce 1996) and its efferent organization as
judged by electrically elicited saccades (Russo and Bruce
1993
). The present study builds on this model of SEF function
by further examining the types of SEF presaccadic neurons, the
relationship between visual and motor response fields, the relationship
between neural response fields and the metrics of saccades elicited by
electrical stimulation at their recording sites, and the local and
global topography of saccade representations across SEF cortex. Our
analyses were based on data obtained from the low-threshold SEF, that
is, the region from which electrical stimulation at low currents
reliably elicits a saccade.
To summarize, we found that neurons in SEF share several properties with both the superior colliculus (SC) and the frontal eye field (FEF). Like these regions, SEF has a representation of saccades to virtually all points in the contralateral visual hemifield, and each neuron and site appear to code a specific saccade vector. SEF contains neurons with purely visual activity, purely movement activity, and both visual and movement activity. When visuomovement neurons were analyzed, the visual and response fields were generally congruent, as is true of visuomovement neurons in SC and FEF. When neurons and elicited saccades at the exact same site were studied, the response fields of the neurons matched the metrics of the saccades subsequently elicited with electrical stimulation, revealing a direct functional linkage between the activity of groups of SEF neurons and the generation of specific saccadic eye movement metrics. Finally, SEF visual activity, movement activity, and its efferent (elicited saccade) organization, have a columnar arrangement with respect to polar direction. Polar direction is generally a continuous representation across the SEF surface; however, it is not a singular representation as in the SC. Instead polar direction appears to be cyclically represented in a hypercolumnar fashion as in FEF. These results and some of their implications are discussed in the following text.
Common functional properties of SEF, FEF, and SC
Overall SEF appears to code specific saccade metrics via the
activation of locally organized groups of neurons that project to
downstream oculomotor centers in a topographic manner. In this respect,
SEF seems remarkably similar to both the primate SC and FEF. Indeed,
the present results show that SC and FEF share many of the same
neurophysiological properties of SEF. For example, both the SC
(Schiller and Stryker 1972; Wurtz and Goldberg
1972
) and FEF (Bruce and Goldberg 1985
) contain
neurons with purely visual activity, purely movement activity, and both
visual and movement activity. In our study, we showed that single SEF
neurons could also be classified on this basis, and the composite
activity in SEF during saccades followed this pattern. Furthermore
neurons in SC (Schiller and Stryker 1972
; Sparks
and Mays 1980
; Sparks et al. 1976
; Van
Opstal et al. 1990
; Wurtz and Goldberg 1972
) and FEF (Bruce and Goldberg 1985
) discharge
maximally in conjunction with visually guided saccades of a particular
size and direction, indicating that only a specific subpopulation of
neurons are activated in conjunction with a particular saccadic eye
movement. In the present study, almost all SEF neurons had an optimal
direction, and most also had a optimal eccentricity, although this
property could not always be quantified because many SEF neurons were
broadly tuned for eccentricity and often still had strong responses
beyond the maximum eccentricity we could test from central fixation
(33° horizontal and 22° vertical). Moreover the saccade vector
associated with the largest neural response at any particular site in
SC (Schiller and Stryker 1972
; Sparks and Mays
1980
; Van Opstal et al. 1990
; Wurtz and
Goldberg 1972
) and FEF (Bruce et al. 1985
) corresponded to the saccadic vector evoked with subsequent electrical stimulation, supporting a direct causal role for the activity of
specific neuron subpopulations in the generation of particular saccadic
eye movements metrics. The strong correlation we found between the
optimal direction and optimal eccentricity of neural activity and
subsequent direction and amplitude of electrically elicited saccades is
also comparable to the correspondence found in the SC and FEF.
Finally, like the SC and FEF, all possible saccades into the
contralateral visual hemifield seem to be represented within SEF. This
includes vertical saccades, which are represented bilaterally in SEF as
they are in FEF and SC. Interestingly there was a significant trend for
recording sites with nearly vertical response fields to yield elicited
saccades rotated somewhat more horizontal (see Figs. 8 and 9). This
could simply reflect the fact that electrical stimulation activated
only one hemisphere, whereas naturally occurring vertical saccades
would entail SEF activity in the vertical representations of both
hemispheres. It could also reflect current spread into neighboring
columns, representing obliquely contralateral saccades. Regardless,
this can be viewed as a systematic perturbation of electrically
elicited saccades, analogous in some ways to the orbital perturbation
of SEF-elicited saccades, which we previously described and postulated
similar explanations for (Russo and Bruce 1993).1 In
both cases we argue that the small but systematic discrepancy between
the neuronal response field and the elicited saccade vector is
explained by careful consideration of the details and artifactual nature of single-electrode microstimulation. In fact, this systematic contralateral perturbation of saccades elicited at vertical
representations should be canceled by having the monkey fixate
contralateral to the stimulated hemisphere (e.g., site RAB103 of Fig. 6 in Russo and Bruce 1993
). We also would predict a
similar contralateral perturbation at the vertical representations in FEF.
In summary, their common neurophysiological properties suggest that all
three oculomotor structures have at least some common oculomotor
functions that use similar neural mechanisms. Thus SEF, SC, and FEF
specify the dimensions of saccadic eye movements via the activation of
a functionally distinct subset of output neurons that project to
downstream oculomotor structures in a topographic manner. Chemical
inactivation of small zones in SC (Hikosaka and Wurtz
1985; Lee et al. 1988
; Quaia et al.
1998
) and FEF (Dias et al. 1995
) results in
saccadic eye movement deficits into the visual field location
represented by the inactivated region. The present data predict that
inactivation in SEF would produce similar results. Permanent and total
SEF lesions do have much smaller and shorter-lived effects than
permanent, total FEF lesions according to the sensitive synchrony test
used by Schiller and Chou (1998)
; however, this may
simply reflect the much larger overall size of FEF (see following
text), and local inactivation effects might be more
comparable.2
Location and size of SEF
The present study targeted the SEF cortex as discovered by
Schlag and Schlag-Rey (1987), where saccades are
electrically elicited with low-threshold stimulation currents. The
thresholds and latencies of elicited saccades reported here generally
agree with that report and thereby help confirm that we are studying
the low-threshold SEF Schlag and Schlag-Rey (1987)
so
definitely described. However, the estimates of threshold for eliciting
saccades in the present study are conservative relative to
Schlag and Schlag-Rey's report (1987)
because we always
stimulated while monkeys fixated a visual target (to consistently
elicit saccades from the same starting eye position used to map
response fields), whereas they usually stimulated while the monkeys
explored a blank screen. Fixation consistently increases the threshold
for electrically eliciting saccadic eye movements from FEF
(Goldberg et al. 1986
) and elsewhere. We decided to use
sites with thresholds >50 µA because our fixation requirement raises
the thresholds, robust presaccadic activity was present at these
sites, and low thresholds for eliciting saccades were found at other
sites on the same penetration or in other penetrations with the
same or nearby electrode coordinates. Even when the 50-µA criteria
was modestly relaxed, the SEF in the present study were still only
~10-15 mm2, similar to the extent of Schlag
and Schlag-Rey's SEF.
Many other studies of SEF have used similar microstimulation criteria
to locate it (Huerta and Kaas 1990; Mushiake et
al. 1996
; Schlag-Rey et al. 1997
; Tian
and Lynch 1995
, 1996
). However, the small size of SEF reported
in those studies and the present report contrasts with studies of the
dorsomedial frontal cortex (DMFC) wherein a much larger electrically
excitable area has been described (Bon and Lucchetti
1992
; Lee and Tehovnik 1995
; Mann et al.
1988
; Mitz and Godschalk 1989
; Tehovnik
and Lee 1993
; Tehovnik and Sommer 1997
). For
example, using a different set of stimulation parameters that included
400 µA of stimulating current and 400-ms stimulation trains,
Tehovnik and Lee (1993)
elicited saccades from an area
~50 mm2. They report saccadic "termination
zones" that were contralateral when rostral sites were stimulated and
straight-ahead or ipsilateral when caudal sites were stimulated. Given
their stimulation parameters and absence of eye movement records, it is
unclear whether just one saccade or multiple saccades was made.
Regardless, it is possible that the low-threshold SEF studied in the
present paper corresponds to (or at least lies within) the rostral area
of Tehovnik and Lee (1993)
; however, as shown in
Russo and Bruce (1993)
, saccades elicited from the
low-threshold SEF are best characterized as a vectors rather than
contralateral "termination zones."
Topographic organization of SEF
The primate SC presents an exquisite topographic mapping of the
contralateral visual hemifield in its superficial laminae with an
isomorphic mapping of saccades across its intermediate layers
(Robinson 1972). In FEF, saccade size is topographically organized with large saccades represented dorsally and small saccades represented ventrally and in the depths of the arcuate sulcus (Bruce et al. 1985
; Robinson and Fuchs
1969
). The representation of saccade direction is more complex,
however, with small shifts in saccade direction accompanied by small
advances of an electrode down the anterior bank of the arcuate sulcus
and multiple representations of direction across FEF (Bruce et
al. 1985
). In contrast, Schlag and Schlag-Rey
(1987)
characterized SEF as having no topographic organization
but instead appeared to be "patchy," and no subsequent report has
demonstrated topographic mapping in SEF to the contrary.
Our data elaborate on the patchy organization of SEF initially
described by Schlag and Schlag-Rey (1987). Clearly SEF
has a columnar organization with respect to polar direction. For both presaccadic activity and electrically elicited saccades, polar direction, which was readily quantifiable, generally remained constant
on a given electrode penetration from the cortical surface down to the
white matter. Of course, some neurons in the column did not have a
presaccadic response. However, such a finding does not detract from a
columnar organization, in the same way that neurons in layer 4 of
striate cortex with concentric receptive fields and no orientation
tuning do not disprove a columnar organization of striate cortex with
respect to orientation. We could not examine the columnar organization
of SEF with respect to response-field eccentricity because independent
measures of response-field eccentricity were seldom obtained at
different recording sites in a single-electrode penetration.
Interestingly, microstimulation was equally effective at eliciting
saccades in SEF regardless of the type of presaccadic activity (visual
or movement) recorded at the stimulation site. This finding contrasts
with FEF, where the lowest thresholds were found at sites of neurons
with movement activity (Bruce et al. 1985). We are not
sure why SEF did not exhibit this property. Perhaps the slightly higher
currents generally used in the present study stimulate a greater volume
of cortical tissue, reducing the importance of exactly where the
microelectrode tip resided. This explanation is consistent with our
finding that visual, visuomovement, and movement SEF neurons did have
significantly different cortical depth distributions, perhaps because
single-neuron recording has a much finer spatial resolution than
electrical stimulation.
Polar direction was organized across the SEF tangential dimensions as well, but not simply. When the topography of saccade direction in each SEF was analyzed, we found zones where direction changed in a fairly monotonic manner for a few millimeters. These progressions were statistically significant despite the presence of some large discrepancies (which could reflect small differences in the electrode's actual cortical entry point between experimental sessions). However, these sequences did not encompass the entire SEF. Instead our data seemed more indicative of a hypercolumnar or cyclical organization of polar direction with multiple representations for some or all directions, similar to how saccades seem to be represented in FEF. Resolving this issue will be challenging because the low-threshold SEF is so small, and its location makes electrode penetrations parallel to the cortical surface difficult.
We did not find any systematic changes in either the optimal
eccentricity of neural response fields or the amplitude of electrically elicited saccades. However, the same difficulties in studying the
topographic organization of saccade direction applied to saccade amplitude as well. Furthermore the range of saccade size represented in
SEF seems more constricted than in FEF. In the present study, the size
of saccades elicited from SEF ranged from 1.8 to 26.9°, with 78% of
the SEF sites between 5 and 20°. In contrast, Bruce et al.
(1985) found that the size of FEF elicited saccades ranged from
<1 to >30°, and Fig. 2 of MacAvoy et al. (1991)
shows that such extremely large and extremely small elicited saccades
can be obtained on a single-electrode penetration through FEF. Such a
difference would not be too surprising given the small size of SEF
(<10 mm2) compared with FEF (~ 100 mm2). Another possibility, however, is that
saccade size is coded in part by the duration of presaccadic bursts.
More research is needed to resolve these issues.
Does SEF have a unique role in saccade generation?
The present study finds that SEF, FEF, and SC use similar neural
mechanisms for generating saccadic eye movements. The existence of
multiple oculomotor areas, however, suggests that each structure evolved to solve specific problems in oculomotor control. As a result,
several functional specializations for SEF have been proposed. For
example, Schlag and Schlag-Rey (1987) observed that some
SEF stimulation sites yielded elicited saccades that appeared to
converge toward a particular orbital position when evoked from
different initial eye positions, and they hypothesized that SEF codes
saccades in a craniocentric coordinate system. However, a quantitative analysis and comparison of saccades elicited from both SEF and FEF
using the same methods in the same monkeys showed that the average
convergence of saccades elicited with SEF stimulation was modest and
did not significantly differ in this regard from saccades elicited with
FEF stimulation (Russo and Bruce 1993
). Furthermore SEF
response-field mapping from multiple eye positions showed that overall
SEF neural activity coded saccades as oculocentric displacements
relative to the current point of fixation (Russo and Bruce
1996
) similar to the FEF, SC, parietal eye field in the
intraparietal sulcus and the saccade generator circuitry in the
reticular formation of the midbrain and pons. Although a craniocentric representation of saccades may seem an adaptive proficiency in some
situations, it may be more critical for the network of interconnected saccadic structures to converse using the same neural code. In fact,
the current study indicates that the basic functional activity in the
SEF is remarkably similar to SC and FEF.
More recently other specializations of SEF have been proposed.
Olson and Gettner (1995) reported SEF neurons with
"object-centered direction selectivity". Chen and Wise
(1995a
,b
, 1996
, 1997
) reported that SEF neurons are most active
during conditional oculomotor learning and that some SEF neurons change
their optimal direction within the context of a conditional oculomotor
learning task. A special role in learning has also been described to
the larger dorsomedial frontal cortex region by others (e.g.,
Mann et al. 1988
). It has also been hypothesized that
SEF has a special role in generating internally guided as opposed to
sensory-guided saccades. For example, there is evidence in humans that
SEF is specialized for programming sequences of saccades
(Gaymard et al. 1990
; Müri et al.
1995
) and for controlling saccades made during head or body
movements (Pierrot-Deseilligny et al. 1993
).
Schlag-Rey et al. (1997)
found that SEF neurons
responded especially vigorously for
antisaccades.3
These hypotheses suggest that the efferent output of SEF is relatively independent of its visual inputs. The close alignment between visual and movement response fields of SEF visuomovement neurons demonstrated in the present report seems contrary to this idea; however, the neural activity used to construct visual and movement response fields was clearly generated independently. Thus their alignment may merely reflect the default option of simple visually targeted saccades. Whether or not the alignment of visual and movement response fields are altered during performance of tasks where the visual stimuli instructing saccades and the saccades themselves are dissociated (e.g., anti-saccades or learned-saccades) or whether cortical connectivity between visually responsive and movement-related neurons is modified without actually shifting response fields is unclear. Obviously such an experiment would necessitate careful measurement of response fields in experimental and control (visually guided) conditions.
Another line of study is suggested by the idea that the evolution and
functional specializations of multiple oculomotor areas is dictated by
the functional specializations of the different skeletalmotor regions
lying adjacent to it (Bruce 1990). Skeletal movements
are orders of magnitude more complex than saccadic eye movements, and
there are now known to be several somatic movement fields located in
the frontal and parietal lobe (reviewed in Kalaska et al.
1997
). SEF may have evolved because the medial skeletal-motor areas were too distant from FEF. Another possibility is that SEF is
primarily concerned with only medium-sized eye movements that are made
in conjunction with forelimb movements and not fine eye movements
concerned with intensive visual analysis nor large eye movements in
response to visual and auditory targets in the far periphery. Such a
supplementary function may be reflected in the relatively small size of
SEF. Understanding the nature of SEF response fields and their exact
relationship to the eye movements generated by their outputs will
facilitate the design and interpretation of studies concerning these
and other functions of SEF.
![]() |
ACKNOWLEDGMENTS |
---|
We thank Optical Coating Laboratory for providing the conductive glass panel used to block interference from the video monitor and G. Leydon for providing software for parts of the data analysis. We also thank H. Friedman for critical comments on the manuscript. G. S. Russo thanks F. Claman for loving support.
National Eye Institute Grant EY-04740 supported this work.
Present address of G. S. Russo: Dept. of Neurology, Emory University School of Medicine, Suite 6000, WMRB, PO Drawer V, Atlanta, GA 30322.
![]() |
FOOTNOTES |
---|
Address for reprint requests: C. J. Bruce, Section of Neurobiology, Yale University School of Medicine, 333 Cedar St., Rm. C303 SHM, PO Box 208001, New Haven, CT 06520-8001 (E-mail: charles.bruce{at}yale.edu).
1
Again, others have interpreted these perturbations as
evidence for a goal-directed saccade representation in SEF, as we
discussed elsewhere in this paper and by Russo and Bruce (1993,
1996
).
2
However, Sommer and Tehovnik (1999) found
that reversible inactivation of macaque "dorsomedial frontal
cortex" had much smaller effects on oculomotor performance than
similar inactivation in FEF.
3
Furthermore SEF function may not solely concern
saccades. Mushiake et al. (1996) and Bon and
Lucchetti (1991)
suggest that SEF may be specialized
for combined arm-eye movements, and there are reports of SEF neural
activity in conjunction with smooth pursuit eye movements
(Heinen and Liu 1997
) and smooth eye movements elicited
with electrical stimulation of SEF (Tian and Lynch
1995
).
Received 6 May 2000; accepted in final form 8 August 2000.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|