Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892
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ABSTRACT |
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Ferraina, Stefano, Martin Paré, and Robert H. Wurtz. Disparity Sensitivity of Frontal Eye Field Neurons. J. Neurophysiol. 83: 625-629, 2000. Information about depth is necessary to generate saccades to visual stimuli located in three-dimensional space. To determine whether monkey frontal eye field (FEF) neurons play a role in the visuo-motor processes underlying this behavior, we studied their visual responses to stimuli at different disparities. Disparity sensitivity was tested from 3° of crossed disparity (near) to 3° degrees of uncrossed disparity (far). The responses of about two thirds of FEF visual and visuo-movement neurons were sensitive to disparity and showed a broad tuning in depth for near or far disparities. Early phasic and late tonic visual responses often displayed different disparity sensitivity. These findings provide evidence of depth-related signals in FEF and suggest a role for FEF in the control of disconjugate as well as conjugate eye movements.
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INTRODUCTION |
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Eye movements permit primates to explore their
visual environment. Conjugate movements that move the two eyes equally
bring the visual axes to a new point at the same depth of fixation, but
disconjugate movements are necessary every time the visual images are
at different depths. These two types of eye movements are controlled by
the saccadic and vergence systems that normally interact to subserve
binocular vision, as demonstrated by recent behavioral studies
(Chaturvedi and van Gisbergen 1998; Erkelens et
al. 1989
; Maxwell and King 1992
; Zee et
al. 1992
).
The neurophysiology of the conjugate saccadic system in both cortical
and subcortical structures has been studied extensively (for reviews
see Wurtz and Goldberg 1989). However, less is known about the neural system involved in the generation of disconjugate eye
movements. Some important vergence centers have been identified in the
midbrain (Judge and Cumming 1986
; Mays
1984
; for a review see Mays and Gamlin 1995
),
but there is scant knowledge about cortical areas playing a definitive
role in the control of disconjugate eye movements. One hypothesis, not
fully tested, is that some of the cortical areas known to be involved
in the generation of conjugate saccades also play a role in the
production of disconjugate eye movements.
Depth discrimination is a prerequisite for correct foveation of visual
stimuli located in three-dimensional space. The most important depth
cue is retinal image disparity, which results when visual images at
different depths in the field impinge onto the two retinas at different
positions (Fig. 1A). Among the
neural structures forming the interface between the visual and saccadic systems, the lateral intraparietal (LIP) area has been shown to contain
disparity-sensitive neurons (Gnadt and Mays 1995).
Moreover, this depth-related signal is carried by LIP output neurons
projecting to two other major visuo-saccadic centers, the midbrain
superior colliculus (SC) (Gnadt and Beyer 1998
) and the
frontal eye field (FEF) in frontal cortex (Ferraina et al.
1999
). Further preliminary data suggest that the FEF may also
be involved in the control of disconjugate eye movements. First,
Jampel (1960)
reported that stimulation of the frontal
lobe could elicit both saccadic and vergence eye movements. Second,
Gamlin et al. (1996)
identified neurons in a prearcuate
area that displayed activity related to tracking in depth. Given these
data and the strong anatomic connections between area LIP and FEF (for
a review see Schall 1997
), we investigated whether the
visual activation of FEF neurons is tuned in depth and thereby possibly
involved in the visuo-motor processes underlying disconjugate eye
movements.
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METHODS |
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Two male monkeys (Macaca mulatta) were prepared for
chronic recording of single-neuron activity and of the positions of
both eyes in a single surgical procedure described previously
(Munoz and Wurtz 1993). All animal care and experimental
procedures were approved by the Institute Animal Care and Use Committee
and complied with Public Health Service Policy on the humane care and
use of laboratory animals.
The anterior bank of the arcuate sulcus was delimited with the help of magnetic resonance imaging (MRI) of the monkey's brain. The exact location of FEF was identified physiologically by the concentration of neurons with visual and saccade-related activities and by the ability to evoke saccades with <50 µA current.
All tasks were performed in dim ambient light with visual stimuli
(single dots, 0.25° diam) generated by a video projector and
back-projected onto a translucent tangent screen positioned 57 cm in
front of the head-restrained monkey. First, we determined the location
of the receptive field and the discharge properties of each isolated
neuron using visual and memory delayed saccade tasks (Paré
and Wurtz 1997). Each trial started with the appearance of a
central visual fixation point and after 500-800 ms of fixation an
eccentric visual target appeared and remained present either for 100 ms
in the memory trials or throughout the visual trials. After a 500-1000
ms delay period, the fixation point disappeared signaling the monkey to
make a saccade to either the remembered location of the target or the
still visible target. Following this classification, the disparity
sensitivity of each neuron was tested using a visual fixation task. To
produce disparity stimuli, we divided the tangent screen into two
halves and projected a fixation point and an eccentric visual stimulus
on each half. The visual stimulus appeared after 500-800 ms of
fixation and remained present for 1000 ms. The location of the stimulus
in the visual field was the same that elicited optimal activation in
the delayed saccade tasks but, this time, maintained fixation was
required. A base-cut prism positioned in front of each eye deflected
the line of sight of the right eye to the right, and that of the left
eye to the left (Eifuku and Wurtz 1999
). Retinal disparity was induced by changing the relative position of the visual
stimuli displayed on the half screens and, to survey a broad range of
disparity, it varied from
3 to +3° in steps of 1°. Different
disparity values were presented in a random order. The fixation point
was always on the screen at 0° disparity (Fig. 1A). With a
57-cm screen distance and an interocular distance of 3.5 cm, the
uncrossed disparity stimuli of +1, +2, and +3° appeared to be
located, respectively, at 22.7, 75.2, and 330.8 cm beyond the plane of
the screen (far). Crossed disparity of
1,
2, and
3° created a
binocular stimulus located 12.6, 20.7, and 26.3 cm in front of the
plane of the screen (near). Throughout the trial, the monkey maintained
fixation with both eyes within a computer-controlled window of
±1-1.5°. Adequate fusion of the fixation stimuli was
inferred by the consistency from trial to trial of the position of both
eyes within the electronic window.
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RESULTS |
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Using the data collected in the visual and memory delayed saccade
tasks, we separated our sample of 57 FEF neurons (36 from monkey C and
21 from monkey A) into different groups with a classification scheme
similar to that used in previous descriptions of FEF neurons (Bruce and Goldberg 1985; Segraves and Goldberg
1987
). Most neurons (n = 35) displayed a
target-locked visual response that usually continued throughout the
delay epoch and a presaccadic increase of activity in either visual or
memory trials; these were classified as visuo-movement neurons (Fig.
1B). In contrast, the activity of visual neurons did not
show a presaccadic increase (n = 11), whereas movement
neurons had only saccade-related discharges (n = 11).
None of the 11 movement neurons showed an emergent visual response for
any of the disparity values tested. We studied the disparity
sensitivity of the 46 neurons that had visual responses. All the
neurons had a large receptive field centered in the contralateral visual field. Because of the optics of the prisms and the display arrangement in the fixation task we were limited to testing visual receptive fields with eccentricities <15°. Of these, seven were judged online to show no modulation with disparity changes. The remaining 39 neurons were examined quantitatively.
Figure 1C shows the responses of a typical visuo-movement neuron (same as Fig. 1B) in the disparity task. Neuronal activation following stimulus presentation consisted of an early phasic response and a later tonic response. Both responses with the far stimuli were stronger than with the near stimuli. However the changes in the two responses associated with the change in disparity were not identical. To quantify this neuronal activity, we measured the discharge rate during an early visual epoch lasting 50-200 ms after target onset and a late visual epoch 300-1000 ms after target onset and compared them across different disparities. In the example of Fig. 1C, both the early and the late visual responses were significantly different during at least one disparity value [Kruskal-Wallis analysis of variance (ANOVA) on ranks, P < 0.05]. Across our sample of visually responsive neurons, the activity of 80% of the neurons (31/39) was significantly modulated by changes in retinal disparity during at least one of the two analysis epochs; 46% (18/39) during both epochs. If we took into account the seven neurons that were qualitatively judged to be nonmodulated, about two-thirds (31/46) of the visually responsive neurons could be considered sensitive to disparity.
The lower traces in Fig. 1C show horizontal positions for the two eyes during fixation of the stimulus at different disparities. We saw no evidence of systematic changes in the position of the two eyes, either on successive trials or between the early and late visual epochs of the trials. In other words, the visual stimulation never elicited minute vergence eye movements.
Figure 2 illustrates the variation in the disparity tuning for both the early and the late visual epochs. The example neurons in Fig. 2A (same neuron as in Fig. 1, B and C) and 2B showed broadly tuned responses that were strongest with far disparities. In addition, both neurons displayed early and late responses that were different, although the responses maintained the same depth preference (far) even when the optimal disparity values differed (Fig. 2B). This similarity in depth preference (near or far) was true for all but three of the neurons studied (36/39). Each of these latter three neurons had a sharp tuning curve centered at zero disparity in one of the two analysis epochs. Figure 2C illustrates one such neuron.
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To estimate the strength of the depth tuning, we first computed the
mean discharge rate for the three far disparities and for the three
near disparities. Then, using these two rate values, we calculated the
disparity index previously employed by Roy et al.
(1992): Disparity Index = 1
(N
C)/(P
C) where P
(preferred) is the highest rate obtained for either the near or the far
disparities, N (nonpreferred) is the lowest rate value
obtained, and C (control) is the average discharge rate
during the final 300-ms fixation before target onset. The larger the
disparity index, the larger the difference in the response to near and
far disparities. For example, the disparity indices for the neuron in
Fig. 2A for the early and late visual epochs were 0.19 and
0.75, respectively.
Figure 3 shows the range of values of the
index for the early and late visual epochs and the relation between
them for all neurons examined (excluding the three neurons with a sharp
zero tuned response). Ninety-seven percent (35/36) of the neurons
showed a disparity index >0.20 (i.e., >20% change in activity)
during at least one of the two analysis epochs. The mean disparity
index for the early and the late visual epochs was 0.44 and 0.60, respectively; not a statistically significant difference (paired
t-test; P = 0.14). However, there frequently
was a substantial difference between the early and the late indices of
individual neurons. Of all the neurons with disparity indices >0.2,
most displayed a broad tuning and could qualitatively be classified as
either far (e.g., Fig. 2, A and B) or near (e.g.,
Fig. 2C, LV epoch) neurons (Poggio and
Fisher 1977). In our sample, neurons tuned for far disparities
predominated (70% of both the early and the late visual responses).
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DISCUSSION |
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We found that many visually responsive FEF neurons were sensitive to retinal disparity. Most of them were broadly tuned in depth, and the disparity tuning of the early and late visual activation often exhibited different profiles.
Neurons showing disparity sensitivity have been found in the primary
visual area (V1) (Poggio and Fisher 1977) and in many other extrastriate visual areas, including the middle temporal (MT)
area (Maunsell and Van Essen 1983
) and the medial
superior temporal (MST) area (Eifuku and Wurtz 1999
;
Roy et al. 1992
) (for a review see Poggio
1995
). In addition, neurons in parietal area LIP are tuned in
depth (Gnadt and Mays 1995
). Because FEF is anatomicly connected with MT, MST, and LIP (Schall et al. 1995
), it
is not surprising to find a depth signal in FEF neurons as well.
Nevertheless, the FEF is the first frontal motor area in which such a
visual property has been demonstrated.
The existence of depth-related signals indicates a possible function
for FEF in shifting fixation to visual stimuli located in
three-dimensional space. The predominance of broadly tuned neurons
suggests a role in the processing of coarse disparity (Bishop
and Henry 1971), which could be important for initiation of
vergence movements because it carries information about the target
distance relative to the fixation point (Poggio and Fisher 1977
). Fine disparity, in addition to its role in stereoscopic perception, may instead be involved in guiding the completion of
vergence and the maintenance of binocular fixation (Poggio 1995
). In addition to disparity, representation of depth could be extracted from other physical parameters of the visual stimulus (e.g., size, blur). FEF neurons could thus be generally sensitive to
depth just as has been shown for antecedent cortical areas (Gnadt and Mays 1995
; Sakata et al. 1985
;
Zeki 1974
), a hypothesis that remains to be tested.
The depth tuning of the early phasic and late tonic response was frequently different. This discrepancy could simply be explained by the fixation task not engaging optimally the visuo-motor functions of FEF neurons. Alternatively, it could potentially indicate a differential participation of these two phases in the visuo-motor process for the generation of disconjugate movements. Perhaps the phasic response is more related to the localization of the saccadic goal in three-dimensional space, whereas the tonic activation is more related to the later processes leading to disconjugate movement execution. Information about the disparity tuning of the movement-related activity may provide further support for this hypothesis, but it is not available from this study because of limitations in the method used for disparity testing.
Our results in FEF along with those obtained in area LIP (Gnadt
and Mays 1995) suggest that these two major cortical areas involved in saccade production probably have a role in the guidance of
disconjugate eye movements. Moreover, just as the saccade-related neurons in the SC intermediate layers may receive a depth-related signal from LIP (Gnadt and Beyer 1998
), the same signal
could be provided by visually responsive FEF neurons, some of which project to the SC (Segraves and Goldberg 1987
;
Sommer and Wurtz 1999
). The identification, in a
complementary study (Ferraina et al. 1999
), of one FEF
disparity sensitive neuron as an SC projection neuron, indicates that
this is indeed likely. Altogether, these data strongly imply that the
SC could be involved in the generation of disconjugate movements (see
also Chaturvedi and van Gisbergen 1999
). Furthermore,
since LIP neurons projecting to FEF also are sensitive to stimulus
disparity (Ferraina et al. 1999
), LIP, FEF, and SC
probably form a network for the control of disconjugate as well as
conjugate eye movements.
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ACKNOWLEDGMENTS |
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We thank the Laboratory of Diagnostic Radiology Research for magnetic resonance images.
S. Ferraina was supported by a Human Frontier Science Program Organization fellowship.
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FOOTNOTES |
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Address for reprint requests: S. Ferraina, Laboratory of Sensorimotor Research, NEI/NIH, 9000 Rockville Pike, Bldg. 49, Room 2A50, Bethesda, MD 20892-4435.
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 27 August 1999; accepted in final form 24 September 1999.
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REFERENCES |
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