Department of Psychology, Green Hall, Princeton University, Princeton, New Jersey 08544
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ABSTRACT |
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Nakamura, K., H. H. Chung, M.S.A. Graziano, and C. G. Gross. Dynamic representation of eye position in the parieto-occipital sulcus. Area V6A, on the anterior bank of the parieto-occipital sulcus of the monkey brain, contains neurons sensitive both to visual stimulation and to the position and movement of the eyes. We examined the effects of eye position and eye movement on the activity of V6A neurons in monkeys trained to saccade to and fixate on target locations. Forty-eight percent of the neurons responded during these tasks. The responses were not caused by the visual stimulation of the fixation light because extinguishing the fixation light had no effect. Instead the neurons responded in relation to the position of the eye during fixation. Some neurons preferred a restricted range of eye positions, whereas others had more complex and distributed eye-position fields. None of these eye-related neurons responded before or during saccades. They all responded postsaccadically during fixation on the target location. However, the neurons did not simply encode the static position of the eyes. Instead most (88%) responded best after the eye saccaded into the eye-position field and responded significantly less well when the eye made a saccade that was entirely contained within the eye-position field. Furthermore, for many eye-position cells (45%), the response was greatest immediately after the eye reached the preferred position and was significantly reduced after 500 ms of fixation. Thus these neurons preferentially encoded the initial arrival of the eye into the eye-position field rather than the continued presence or the movement of the eye within the eye-position field. Area V6A therefore contains a representation of the position of the eye in the orbit, but this representation appears to be dynamic, emphasizing the arrival of the eye at a new position.
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INTRODUCTION |
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The position of the eyes in the orbits affects the
activity of neurons in a number of cortical areas in the primate brain. For example, in area 7a in the parietal lobe, eye position plays a
modulatory role, increasing or decreasing the responses of the neurons
to visual stimuli (Andersen and Mountcastle 1983;
Andersen et al. 1985
). A neuron in area 7a may be highly
visually responsive when the eyes are in one position and relatively
unresponsive when the eyes are in another position. For other neurons
in the same area, the position of the eyes may influence the level of spontaneous activity. Similar effects of eye position were reported in
area V3a, the lateral intraparietal area (LIP), the parieto-occipital area (PO), the ventral premotor cortex (PMv), area MT, and area MST
(Andersen et al. 1990
; Bremmer et al.
1997
; Boussaoud et al. 1993
; Galletti and
Battaglini 1989
; Galletti et al. 1993
;
Graziano et al. 1994b
). In the dorsomedial frontal
cortex (DMFC), the neurons are influenced by eye position but only when
the monkey is performing a fixation task for a reward (Lee and
Tehovnik 1995
; Tehovnik et al. 1995
).
When the monkey makes spontaneous eye movements, the neurons no longer
fire in association with eye position.
Areas V3a, LIP, 7a, PO, and DMFC are all monosynaptically
interconnected, and PMv is connected to the other areas through multisynaptic routes (Cavada and Goldman-Rakic 1989a,b
;
Colby et al. 1988
; Jones and Powell 1970
;
Kunzle 1978
; Matelli et al. 1986
;
Mesulam et al. 1977
). What is the purpose of this
network of areas, and why do its neurons encode both visual stimuli and the position of the eyes? As Andersen and colleagues (1985)
emphasized, the location of an object with respect to the head can be calculated by
combining information about the position of the visual image on the
retina with information about the position of the eye. Therefore one
possible function of these areas may be to calculate the locations of
objects in space. In support of this view, damage to these areas in the
monkey brain and to comparable locations in the human brain produces a
variety of deficits in processing the spatial locations of stimuli and
in guiding movements toward spatial locations (for reviews see
Andersen 1987
; Gross and Graziano 1995
).
Recently, eye position signals were reported in a region on the
anterior bank of the parieto-occipital sulcus. This region was
originally termed area PO (Covey et al. 1982), but
subsequently PO was restricted to a more ventral part of the sulcal
bank (Colby et al. 1988
). The region just dorsal to the
newly defined PO was termed V6A (Galletti et al. 1996
).
Galletti et al. (1993
, 1995
, 1996
) found that ~65% of neurons in V6A
were visually responsive. Of these, 61% were modulated by the position
of the eyes, in that the visual responses were stronger when the eyes
were in some positions than when the eyes were in other positions. In
addition to this modulatory influence of eye position on the visual
responses, for ~42% of the neurons the spontaneous activity depended
on the position of the eyes.
We further examined the properties of eye-position-dependent neurons
in area V6A in two ways. First, we tested whether the neurons were
influenced by eye position during spontaneous eye movements in the
dark. Second, we tested neurons in both a saccade task and a fixation
task to distinguish activity related to eye position per se from
activity related to the direction of the saccadic eye movement. In the
course of these experiments, we also found that many neurons either in
a subregion of V6A or in an area immediately adjacent to V6A were
influenced by the movement and position of the arm. Galletti et al.
(1997) also described neurons in the parieto-occipital sulcus related
to the movement of the arm but did not report any spatial segregation
between the eye- and the arm-related neurons.
A preliminary account of these experiments was published previously
(Nakamura et al. 1996).
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METHODS |
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Single neuron activity was recorded from four hemispheres of three male Macaca fascicularis (4-6 kg). All husbandry, surgical, and behavioral procedures were approved by the Princeton University Institutional Animal Care and Use Committee and were in accordance with the NIH Guidelines for Care and Use of Laboratory Animals (1985).
Initial surgery
For each monkey, an initial surgical operation was performed
under ketamine anesthesia and strict aseptic conditions, during which
the top of the skull was cleared of skin and muscle, titanium screws
were screwed into the bone, and the exposed bone was covered with a
layer of dental acrylic ~1 cm thick. A stainless steel recording
chamber, 2.5 cm in diameter, was embedded in the acrylic over the
parietal lobe for a vertical approach to the parieto-occipital sulcus.
The approximate location of the sulcus for each monkey was determined
from magnetic resonance images (MRI) (for details of MRI methods see
Moore et al. 1995). A steel bolt for holding the head
was also imbedded in the acrylic. Each animal recovered from the
effects of the surgery within several days but was given 3 additional
weeks to allow the skull to grow tightly around the skull screws. In a
subsequent procedure, also under deep anesthesia and aseptic
conditions, the recording chamber was opened, and a hole ~5 mm in
diameter was drilled through the layer of acrylic and the bone,
exposing the dura.
Recording procedures
During the daily recording sessions, the monkey sat in a primate
chair with its head held in place by the head bolt and with a hydraulic
microdrive (Narishige, type MO-95) mounted on the top of the recording
chamber. A steel guide cannula (an 18-gauge syringe needle) was lowered
through the hole in the skull and into the dura. Then the
varnish-coated tungsten microelectrode (Frederick Haer, impedance
0.5-5 M) was advanced from the guide cannula into the brain to
record from neurons in the anterior bank of the parieto-occipital sulcus.
Once a cell was isolated, as indicated by the repeatability of its wave form on the oscilloscope, it was tested for any response related to the position or movement of the eyes. This was done first by turning off the room lamp and monitoring the neuron while the monkey made spontaneous eye movements in the dark. Eye position was measured with an infrared eye-tracking system (ISCAN Pupil Tracking System, model RK-416, resolution ~0.5°). The neuron was then tested while the monkey performed a fixation task and a saccade task (see Fixation task and Saccade task). Some of the cells were also tested for any response related to the position or movement of the arms (see Reach task). Finally, some cells were tested for visual and somatosensory responsiveness (see Visual and somatosensory stimuli).
Fixation task
The fixation task was performed in darkness. Figure 1A illustrates the events in the task. Each trial began with a warning tone (0.2 s), and then a fixation spot 0.5° in diameter was presented on a multiscan monitor (Liyama Electric, model MF-5221A) placed 28 cm in front of the monkey. For its reward, the monkey was required to fixate the spot within a 4 × 4° electronic window (ISCAN Pupil Tracking System) and maintain fixation until the end of the trial. Two of the three monkeys were trained on a fixation duration of 1.5 s. The third monkey was trained on a fixation duration of 1.2 s but partway through the experiment was promoted to a 1.5-s duration. At the end of the trial, the fixation spot was turned off, a valve released ~0.2 ml of juice into the animal's mouth, and the intertrial interval (ITI) began. The ITI was 1.5-2.5 s. If the animal broke fixation at any time during the trial, the fixation spot was turned off, no reward was given, and the ITI began. Two of the monkeys were trained to press a lever after the warning tone, at the start of the trial, with the contralateral hand, and to maintain pressing until the end of the trial. If the monkey released the lever during the trial, the trial was aborted without a reward, and the ITI began. The purpose of the lever press was to keep the contralateral hand stationary because we found that some neurons were sensitive to the monkey's arm position and arm movement. In this way we could isolate the effects of eye position and eye movement on neuronal activity.
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The fixation spot was presented at 1 of 20 possible positions. These positions were arranged in a 4 × 5 grid and were 12° apart from each other (see Fig. 1C). However, not all 20 positions were tested for every neuron. Usually 18 fixation positions were tested, but some neurons were tested with 9 or 12 fixation positions.
Statistical analysis for fixation task
For each neuron, we analyzed the firing rate (spikes/s) from the period beginning when the monkey's eye first entered the fixation window and ending 1,500 ms later, at the end of the required fixation period. To determine if this firing rate was significantly different for different fixation positions, a one-way Kruskal-Wallis test was performed. For example, the neuron illustrated in Fig. 3 was tested at 18 eye positions, with 10 trials at each eye position. A Kruskal-Wallis test on the 18 groups showed that the firing rate varied significantly with eye position (n = 180, df = 17, H = 6,181, P < 0.0001).
All neurons that showed a significant dependence on eye position with the Kruskal-Wallis test were then tested as follows. The fixation position at which the neuron gave the highest mean spikes/s was selected. The 1.5-s fixation period was then divided into two analysis periods, the first 0.5 s and the subsequent 1.0 s. The data from these two periods were compared with the Wilcoxson nonparametric test for correlated subjects. If the firing rate in the first period was significantly greater than the firing rate in the second period, the cell was considered to have a response that was strongest immediately after the onset of fixation and then decayed over the period of fixation. If the firing rate in the first period was not significantly different from the firing rate in the second period, the neuron was considered to have a response that was sustained throughout the fixation period. None of the neurons responded significantly more in the second period.
Saccade task
In the fixation task described in the previous section, the monkey's eye position and saccadic eye movements before the onset of fixation varied from trial to trial. The saccade task was designed to control these variables. Figure 1B illustrates the events in the saccade task, which was performed in darkness. Each trial began with a warning tone (0.2 s). Then a fixation spot 0.5° in diameter was presented on the monitor. The monkey was required to fixate the spot within a 5 × 5° electronic window and maintain fixation for 0.5 s. Then the fixation spot disappeared, and simultaneously another spot, the saccade target, appeared. The monkey was required to saccade to the target within 1,000 ms and then to maintain fixation on the target for another 1.5 s. At the end of the trial the target spot disappeared, a valve released ~0.2 ml of juice into the animal's mouth, and the 1.5- to 2.5-s ITI began. If the monkey broke fixation during the trial or failed to saccade to the target within the required time, the trial was aborted without a reward, and the ITI began. Two of the monkeys were trained to press a lever after the warning tone, at the start of the trial, with the contralateral hand, and to maintain pressing until the end of the trial. If the monkey released the lever during the trial, the trial was aborted without a reward, and the ITI began.
The saccade target could be presented at one of nine possible positions
(Fig. 1C, ). These positions were arranged in a 3 × 3 grid with 12° separation between each position. The central position for the saccade target was the same as the position of the
fixation point. Therefore, on trials when the target appeared at the
center, the monkey was not actually required to saccade anywhere but
instead to maintain fixation at the same position for the entire trial.
Most cells were tested with all nine saccade target positions, but some
cells were tested with fewer positions. For each neuron, each position
was tested with
10 trials.
In separate blocks of trials, the starting fixation position and the entire set of saccade target positions were shifted to a different location, and the neuron was tested again. In this fashion we could study the effect of eye position on the saccadic activity of the neurons.
Statistical analysis for saccade task
All analyses were performed on the firing rate in the period after the saccade, beginning when the monkey's eye first entered the saccade target window and ending 1.5 s later, at the end of the required fixation period. The reason for using this time period is that for all responsive neurons the response began postsaccadically, after the onset of fixation (see RESULTS). For each neuron, the following statistical tests were performed.
1) Was the activity of the neuron during fixation dependent on the direction of the saccade that preceded fixation? Each fixation position could be approached by many different directions of saccade. We selected the fixation position that gave the largest mean response for that neuron (but some exceptions are described subsequently) and sorted the data into different groups corresponding to the different directions of saccade that were used to approach that fixation position. We then performed a one-way Kruskal-Wallis test to determine if there was any significant difference between these groups. A significant difference would indicate that the firing rate of the neuron during fixation at that position depended significantly on the direction of the saccade that preceded the fixation.
In many cases the neuron preferred a fixation position at the edge of the test grid, which could only be approached by a limited range of saccade directions. In these cases, we selected a fixation position closer to the center of the test grid to test for saccadic dependence. Some neurons did not respond at all near the center of the test grid, and these neurons could not be tested for saccadic dependence.
2) Was the activity of the neuron during fixation dependent on the position of the fixation point? For this test we selected the saccade direction that gave the maximal overall response. We then sorted the data into groups corresponding to the different fixation positions reached by that direction of saccade. We performed a one-way Kruskal-Wallis test on these groups to determine if there was any significant difference between them. For example, Fig. 9 shows the responses of a neuron that preferred downward saccades. Six different fixations positions were approached by a downward saccade (Fig. 9, A-F, bottom positions). We performed a one-way Kruskal-Wallis test on these six conditions and found that the response was significantly different in the different conditions (H = 15.71, P = 0.0004), that is, the response depended significantly on the position of the fixation point.
Some neurons responded equally well to all directions of saccade, and in these cases the data for all saccade directions were combined for this test.
3) Many neurons showed a significant effect of both saccade
direction and eye position, as determined by test 1 and 2. Therefore an
index was calculated to quantify whether the neuron was more "saccade
related" or "eye-position related." We first selected a fixation
position near the center of the test grid that gave the largest mean
response for that neuron and sorted the data into different groups
corresponding to the different directions of saccade that were used to
approach that fixation position. We then calculated the variance
between these groups, VS. A neuron that responds differently
to different saccade directions should have a large value of
VS, and a neuron that is unselective for saccadic direction
should have a small value of VS. In a similar fashion, we
selected the saccade direction that gave the maximal response and
sorted the data into groups corresponding to the different fixation
positions reached by that direction of saccade. We then calculated the
variance between these groups, VP. A neuron that responds
differently to different fixation positions should have a large value
of VP, and a neuron that is unselective for fixation
position should have a small value of VP. Finally, we calculated the index, I = (VP VS)/(VP + VS). For an eye-position cell, that is, a cell that responds in relation to the fixation position and has no dependence on the direction of the saccade, VS will be small compared with VP, and
I ~ 1. For a saccade-related cell with no dependence
on eye position, VP will be small compared with
VS, and I ~
1. For a cell that is
equally influenced by eye position and saccadic direction,
VP ~ VS and I ~ 0.
4) Many neurons showed a clear border between preferred eye positions and nonpreferred eye positions. A nonpreferred eye position was defined as a position at which the neuron gave less than one-half of its response at the most preferred eye position. We tested whether the neuronal response was greater when the eye saccaded from a nonpreferred to a preferred eye position than when the eye saccaded between two positions that were already both within the preferred range. All the data recorded when the eye saccaded from a nonpreferred to a preferred position were grouped and compared with all the data recorded when the eye saccaded from a preferred position to another preferred position. A Mann-Whitney U test was then performed on these two groups to determine if they were significantly different.
Reach task
Many of the neurons in the PO sulcus seemed to respond during movements of the arm. Therefore each monkey was trained as follows. The experimenter held a jeweler's screwdriver in front of the monkey, and the monkey was required to reach out and touch the screwdriver. The experimenter then rewarded the monkey by pressing a button that opened the juice valve and released juice into the monkey's mouth. By using this simple method, any direction or magnitude of reach could be studied. Most of the reach-related neurons were studies in this fashion.
In addition, one monkey was trained to touch illuminated circles on a touch-sensitive screen placed 28 cm away. For this task, the monkey first pressed a lever that was centered and at waist level just in front of its body while also fixating a central fixation spot on the screen within a 4 × 4° fixation window. After 500 ms, the fixation spot disappeared, and a target circle (8 deg in diameter) was presented on the screen. The monkey was required to saccade to the target circle and maintain fixation. Then after a delay of 500 ms the monkey was required to release the lever, reach out with the same hand, and touch the target circle. The task was performed in darkness so that movement of the arm was not visible. This paradigm was used to study only four reaching-related neurons but is described here because it allowed us to collect quantitative data confirming the existence of the reach-related response and showing that it was independent of the sight of the arm, the position or movement of the eyes, and the onset of the target stimulus (see Fig. 13).
Visual and somatosensory stimuli
Visual receptive fields were tested with bars, spots, squares, and complex colored images such as a picture of a monkey's face, back-projected onto a 160 × 160° tangent screen 28 cm in front of the monkey. During stimulus presentation, the monkey performed the same fixation task described previously (fixation task) except that the fixation spot in this case was a light-emitting diode (LED) 1 cm in diameter, taped to the projection screen.
Somatosensory responsiveness was studied with manual palpation, manipulation of joints, gentle pressure, and stroking with cotton swabs.
Behavioral training
Training on all tasks was done with a liquid reward. First the animal's ad lib daily water intake was measured, and based on this measurement the animal was placed on a water schedule in which he received liquids under three conditions only: as a reward (cranberry juice) during the experimental session, as a supplement immediately after each session, and free water for 2 consecutive days each week. Two of three animals were first trained to press a lever with the contralateral hand and hold it for 1.5 s. For the third animal, this step was omitted. All three animals were trained to fixate a central fixation spot for 0.5 s. Next they were trained to fixate any of the 20 positions shown in Fig. 1C. They were then trained to saccade to a target presented just after the offset of the fixation spot. Finally, the fixation time was increased to the full 1.5 s.
Histology
In the last week of recording from each monkey, marking lesions
and iron deposits were made by passing a 20-µA current through a
stainless steel electrode at two different depths at four to six
locations. At the conclusion of recording, the monkey was given an
overdose of pentobarbital and perfused transcardially with saline
followed by 10% formalin. Ferrocynaide (2%) was mixed with the
formalin to color the iron deposits. The brains were serially sectioned
at 100 µm in the coronal place and then stained with cresyl violet.
Electrode tracks were identified with the lesions as reference points.
As shown in Fig. 2A for each
monkey, the recording sites were located mainly in the top one-half of the anterior bank of the parieto-occipital sulcus but also extended onto the dorsal and medial surface of the superior parietal lobe. This
area corresponds roughly to V6A of Galetti et al. (1996). It may
overlap the dorsal border of area PO of Colby et al. (1988)
. The
recording site in monkey AL extended more laterally and anteriorly than
in the other two monkeys and did not include the medial surface of the
hemisphere. Figure 2B shows representative coronal sections through the right parietal lobe of two of three monkeys. Each section
shows a representative track along which electrodes penetrated the
cortex and the region along the track in which neurons were recorded
(thickened portion of track).
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RESULTS |
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Response categories
We studied 354 neurons in 4 hemispheres of 3 monkeys. Table 1 shows the proportions of neurons in each response category. Although 354 neurons were tested, not all neurons were tested for every response property. Table 1 shows the results only for the 187 neurons that were tested for all of the properties listed. "Eye" neurons responded only in relation to the position or movement of the eyes; "visual" neurons responded only to visual stimuli; "arm" neurons responded only to the position or movement of the arm. Other neurons responded under more than one of these conditions (e.g., eye + visual, eye + arm). One neuron had a tactile response over most of the body, strongest on the contralateral hand; this neuron also responded in relation to arm movement. For 11 neurons, we failed to determine the effective stimulus. Most of these "undefined" neurons fired as the monkey moved in the chair.
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Eye-related neurons
Three hundred ten neurons were tested for the effect of eye position and movement, and 149 (48%) responded. Some of these neurons, such as the eye + visual neurons, also had other response properties. Figure 3 shows the responses of a typical eye-related neuron, tested during the fixation task. This cell was most active while the monkey was fixating the top right position (position 12, 24). The elevated firing started after the onset of fixation (indicated by the horizontal line) and was sustained throughout the 1.5-s fixation period. In contrast, the neuron showed little or no firing when the monkey was fixating the other 17 positions. This difference in firing rate between the different positions was statistically significant (Kruskal-Wallis test, H = 6181, P < 0.0001; see METHODS for details).
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Figure 4 shows the response profiles for another 20 typical neurons. Some (Fig. 4, A-D) fired most when the eyes were within a small range of preferred positions and responded less well or not at all to the surrounding positions. Some (Fig. 4, E-H) showed response profiles that increased monotonically from one edge of the test grid to the other. These four examples had discharge rates that increased smoothly as the eyes fixated more toward the top-left (Fig. 4, E), right (F), bottom (G), and top (H). The remaining 12 examples showed a variety of complex response profiles. Almost all of them (Fig. 4, I-R) fired most when the eyes were at the edge of the range that we tested. In these cases, we could not determine if the cell had a peak in the response profile or if the response continued to increase as the eye position became more eccentric.
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Of the 149 eye-related neurons, 83 were tested with at least the
central 9 fixation positions. For each neuron we determined which of
these nine positions gave the greatest response. Figure 5 shows a frequency histogram of the
results. None of the 83 neurons preferred the central eye position.
Instead all responded better to eye positions that were deviated from
the center of gaze. This tendency was highly statistically significant
(2 test, P < 0.001).
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The results presented so far suggest that the eye-related neurons in V6A encode the position of the eye during steady fixation. However, at least two alternative hypotheses remain to be tested. First, the activity of these neurons might be caused by the visual stimulation of the fixation spot. Second, the activity might represent the timing or direction of the saccadic eye movement that brought the eye to the fixation position. In the following sections we examine these two alternative hypotheses.
Eye position or visual response?
The eye-related neurons in V6A responded when the monkey fixated
on a spot of light. Was this response caused by the visual stimulation
of the fixation spot? For example, the cells might have a visual
response that is stronger for some eye positions and weaker for others.
Such modulation of the visual response by eye position is common in
this brain area (Galletti et al. 1993, 1995
, 1996
).
However, two control tests demonstrated that the responses of the
eye-related neurons were not dependent on the fixation light. First,
the neurons responded in darkness during spontaneous eye movements. For
example, consider the neuron that is shown in Fig. 3. This neuron was
most active while the monkey fixated the top right position (position
12, 24). Figure 6 shows the result for
the same neuron when the monkey sat in the dark and did not perform any
task. No fixation light was presented. Each tic mark represents an
action potential, and the horizontal lines indicate the time during
which the monkey was looking within 5° of the preferred eye position
for the cell. The neuron fired at a high rate when the eyes were within
this preferred position. Thus neither the presence of a fixation light
nor the performance of a fixation task was necessary to make the cell
respond. All of the eye-related neurons responded during spontaneous
eye movements in the dark, in a fashion that matched the responses
during the parametric tests.
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Second, we tested the effect of blinking off the fixation light while the monkey was fixating. Figure 7 shows the result for a cell tested at its preferred eye position. In Figure 7A, the fixation light turned on and remained on while the monkey fixated for 1.5 s. The neuron's firing rate increased after the onset of fixation and was sustained throughout the entire fixation period. In Fig. 7B, the fixation light turned on, the monkey fixated for 1.5 s, but the light was extinguished for 0.4 s during the period of fixation. The neuron did not show any decrease in firing when the light was extinguished. We compared the data during the 0.4 s that the light was extinguished with the data during the subsequent 0.5 s with the Wilcoxson test for correlated data and found that there was no significant difference in the neuronal activity between these two time periods (T = 21, P = 0.51).
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Fifteen eye-related neurons were tested in this fashion, and the firing of all 15 neurons remained constant even while the fixation spot was turned off, as long as the eye was still fixating the preferred position. These results show that the activity of the eye-related neurons was not due to the visual stimulation of the target spot.
Eye position or saccadic vector?
Does the activity of eye-related neurons reflect the position of the eye during fixation, or does it reflect the vector of the saccade that brought the eye to that position?
Figure 8 shows the results for a neuron
tested in the saccade task. In Fig. 8A, the monkey fixated
the central position (0,0) and then saccaded to one of four surrounding
positions, 12° up, down, right, or left. The central histogram (0,0)
shows the result when the monkey did not make a saccade but maintained
fixation at the initial location. The neuron did not respond under this condition. Instead, the neuron responded best when the monkey saccaded
to the top position (0,12) and the rightward position (12,0). The
response began after the eye reached the target position. Did this
activity reflect the saccadic vector that preceded fixation, that is,
was it caused by an upward and a rightward saccade, or was it an
eye-position response, caused by the final position of the eye after
the saccade was completed? To answer this question we changed the
initial fixation position and then retested the cell. In this second
test (Fig. 8B), the monkey fixated a new starting position
(12,12) and then saccaded to one of four surrounding target positions.
Under these conditions, the cell responded best when the eye saccaded
to the leftward position (0,12) and the downward position (12,0). These
are the same two positions that elicited a response previously, that
is, the firing of the cell depended on the final position of the eyes,
not on the direction of saccade that preceded the fixation. Indeed,
each direction of saccadeup, down, right, or left
elicited a
response when it terminated at a preferred position; likewise, no
direction of saccade gave a response when it terminated at a
nonpreferred position. (The dependence on eye position was significant:
test 1, H = 22.64, P < 0.0001. The
dependence on saccade direction was not significant: test 2, H = 1.029, P = 0.794. See
METHODS for details. See also next section for more data on
and further analysis of this neuron.)
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Figure 9 shows the results for a second
neuron. In Fig. 9A, the monkey fixated an initial position
(12,12) and then saccaded to one of four surrounding positions. This
cell responded best after the monkey saccaded downward and leftward.
Figure 9, B-F, shows the result when the initial
fixation position was changed. In every case, the neuron preferred the
same direction of saccade, that is, downward and leftward. This neuron
therefore responded in relation to saccadic vector. In addition, the
magnitude of the response was modulated by the position of the eyes.
The response was larger in Fig. 9, A and D, when
the eyes were deviated toward the left side of the screen, and smaller
in C and F, when the eyes were deviated toward
the right side of the screen. These data show that both eye position
and the direction of saccadic eye movement influenced the activity of
this neuron. (Dependence on eye position was significant: test 1, H = 43.69, P < 0.0001. Dependence on
saccade direction was significant: test 2, H = 15.71, P = 0.0004.)
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Forty-six eye-related neurons were tested with multiple starting positions in the saccade task. Of these, 19 responded only at the extreme edge of the test grid and therefore could not be analyzed for saccadic and eye-position dependence (see METHODS). Of the remaining 27 neurons, all were significantly affected by the position of the eye during fixation. These cells responded significantly better at some fixation positions than at others. Eighteen of these cells (66%) also responded in relation to the direction of saccade that preceded fixation.
For all 46 neurons tested, the response began after the eye entered the final fixation window. None of the cells, not even the 18 cells that were dependent on saccadic vector, responded before or during the saccadic eye movement.
For each neuron we calculated an index to quantify whether the neuron
was more dependent on saccade direction or on eye position. An index of
+1 indicates that the response of the neuron is dependent solely on
fixation position; an index of 1 indicates that the response is
dependent solely on saccade direction; and an index of 0 indicates that
the response is equally dependent on both (see METHODS).
For example, the neuron in Fig. 8 had an index of 0.89, indicating that
it was highly dependent on eye position and not on saccade direction.
The neuron in Fig. 9 had an index of 0.18, indicating that it was
approximately equally dependent on eye position and saccade direction.
Figure 10 shows the results for all 27 neurons tested. The distribution is skewed toward 1. The index ranges
from
0.33 to +0.96, and only five neurons (19%) had negative
indices. The population of neurons is therefore more influenced by eye
position than by saccade direction.
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Steady-state eye position, or saccades to a preferred eye position?
Figure 11 shows data from the same neuron illustrated in Fig. 8. As described previously, this neuron had an eye position field that encompassed positions 0,12 and 12,0. When the eye saccaded into this region, the neuron responded. The histograms in Fig. 11, however, show that, if the eye was already in the eye position field and then saccaded to a second location also within the eye position field, the neuron responded less well. That is, the neuron was most sensitive to the movement of the eyes into the borders of the eye position field and relatively insensitive to the movement of the eyes within the borders.
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In Fig. 11A, the monkey fixated three different starting
positions and then saccaded to position 12,0, inside the cell's eye position field. The cell responded best when the starting positions were 0,0 or 12,12, outside the eye position field. The response just
after the arrival of the eyes almost disappeared when the starting
position was already inside the eye position field, at 0,12. In Fig.
11B, the monkey fixated five different starting positions and then saccaded to position 0,12, inside the eye position field. Again, the only condition that elicited little or no response was when
the starting position for the eye was already inside the eye position
field, at 12,0. A Mann-Whitney U test showed that the
responses when the eye began outside and then entered the eye position
field were significantly greater than the responses when the eye began
and ended in the eye position field (Z = 6.64; P < 1 × 107; the Z
value was used instead of the U value because of the large sample size; n1 = 20, n2 = 60).
We performed similar tests on 22 neurons with eye position fields. For 18 neurons (82%), the response was significantly larger when the eyes started outside the eye position field and then saccaded to a point inside the eye position field. These results indicate that the eye-related neurons in area V6A preferentially code the arrival of the eyes into the eye-position fields.
A related property is that many of the neurons tested in the fixation task or the saccade task (53/118 cells, 45%) responded best or only within the first 500 ms of fixation. For these cells the firing rate dropped significantly in the subsequent 1,000 ms of fixation (see METHODS for statistical details). These cells therefore appear to emphasize the initial arrival of the eyes at the preferred position, that is, they preferentially code a change in status rather than a steady state.
Visually responsive neurons
Three hundred thirty-four neurons in V6A were tested for visual responsiveness, and 73 (23%) responded. Of these, 56 were exclusively visual, and 17 also had other response properties, such as eye-position or reaching-related responses. One type of visual neuron that we found responded to the fixation spot during the fixation task. Figure 12 shows the responses of one of these cells. This neuron did not respond during spontaneous eye movements in the dark and therefore was not classified as an eye-related neuron. In Fig. 12A, the fixation light turned on and remained on while the monkey fixated on it for 1.5 s. The neuron responded during this period of fixation. In Fig. 12B, the light was extinguished for 0.4 s during fixation. The neuron stopped responding when the light was turned off. Therefore the cell responded to the visual stimulation caused by the fixation light. This pattern of response is quite different from the pattern for eye-related neurons (see Fig. 7).
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Many of the visual neurons also responded to the onset of a room lamp or to moving or stationary bars projected onto a tangent screen. We did not systematically plot visual receptive fields or systematically test if the visual responses were modulated by eye position.
Arm-related neurons
Of 263 neurons tested, 56 (21% of total) responded in association with the movement or position of the contralateral arm. We found these neurons unexpectedly during the first months of the experiment and studied them qualitatively, training the monkey to reach toward a target that was held in the experimenter's hand; therefore we do not know the precise parameters of their responses. However, the relatively high incidence of reaching-related responses suggests that these neurons form an important part of the makeup of this portion of the parietal lobe. The following observations may help to clarify the nature of their responses. Of the 56 reaching-related neurons, 41 were exclusively related to the arm, whereas 15 also had other properties, such as eye-position-related responses. Some reaching-related neurons (20, 36%) responded only during the arm movement itself and stopped responding after the arm reached its final position, whereas other neurons (36, 64%) continued to respond for as long as the monkey maintained its arm in an outstreched position. The preferred direction of arm movement (toward the contralateral or ipsilateral side) was determined for 42 of the arm-related neurons. Most (27, 57%) responded best when the monkey reached toward the contralateral side, but some responded best to ipsilateral reaching (10, 21%), and some responded equally well to either direction of reaching (5, 11%). The reaching-related neurons were also tested when the monkey's eyes were covered or when view of the arm was blocked through some other means such as with a sheet of cardboard. Under these conditions the neurons still responded during the arm movement, indicating that the neurons were not responding to the visual stimulus of the arm in motion.
Figure 13 shows the responses of a typical reaching-related neuron. In this case, the monkey was trained to reach out with the contralateral hand and touch an illuminated circle on a touch-sensitive screen (see METHODS for details). Eye position was controlled, and the reach was performed in darkness. The monkey reached 20° to the left (Fig. 13A), toward the midline (B), or 20° to the right (C). As shown in the figure, this neuron was most active before the leftward (contralateral) reach and least active before the rightward (ipsilateral) reach.
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Almost all of the arm neurons (46/50, 92%) were found in monkey A. L. As shown in Fig. 2, the recording site in A. L. extended more laterally and also more anteriorly onto the cortical surface of the superior parietal lobe. Most of the arm neurons were found in this lateral, anterior region. In Fig. 2B three representative coronal sections from monkey A. L. are shown. In the most posterior section, 36 neurons were studied, of which only 2 (6%) responded in relation to the arm. In the next example section shown, 0.5 mm more anterior, 21 neurons were studied, of which 13 (62%) responded in relation to the arm. Finally, in the most anterior section, another 1.5 mm anterior, 24 neurons were studied of which 21 (88%) were related to the arm. These results suggest that there may be a separate arm area located anterior to the eye-related neurons in area V6A. However, more extensive mapping studies will be necessary to confirm the existence of an arm area.
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DISCUSSION |
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We found two principal types of neuronal responses in area V6A;
48% of the neurons responded in relation to the movement or position
of the eyes, and 23% responded to visual stimuli. Previous studies by
Galletti et al. (1993, 1995
, 1996
) found that 42% of the neurons
responded in relation to the position of the eyes, and 65% were
visually responsive. In addition, they reported that 61% of the visual
neurons were modulated by eye position, in that the visual responses
were stronger for some eye positions than for others. Although we
encountered the same phenomenon, we did not systematically study it.
We also found neurons that responded in relation to the movement or
position of the arm. These arm-related neurons were located mainly in
what was either a subregion of V6A or an area adjacent to V6A, more
anterior and lateral than the location of most of the eye-related
neurons. Galletti et al. (1997) also reported arm-related activity in
V6A but did not report any spatial segregation between eye neurons and
arm neurons.
A representation of eye position
As described previously, 48% of the V6A neurons in this study were classified as eye related. When tested in a fixation and a saccade task, these cells responded according to the position of the eyes, that is, each cell had a preferred range of eye positions or an eye position field. The responses were not caused by the visual stimulation of the fixation light because when the fixation light was turned off the cells continued to respond. Even when the monkey made spontaneous eye movements in the dark, the firing of these neurons continued to provide an accurate account of the changing position of the eyes. The population of cells in V6A therefore appears to form a representation for eye position.
However, we found that 66% of the eye-position neurons were also influenced significantly by the direction of the saccade that preceded fixation. This sensitivity to the direction of the saccade was surprising because all of the responses were postsaccadic. None of the cells responded before or during saccades.
We suggest that the saccade direction information may contribute to the representation of eye position, that is, it may be used by V6A neurons to help calculate the position to which the eyes just arrived. The next section discusses one way in which saccade information might influence the representation of eye position.
A stronger signal when the eye moves than when the eye is stationary
Many of the eye position neurons (45%) responded best within the
first 500 ms after the eye made a saccade to a preferred position. The
response then dropped off while the eye remained at that position.
These neurons therefore preferentially encoded the arrival of the eye
in the eye position field rather than the continued presence of the eye
in the eye position field. Furthermore, when the starting and ending
point of the saccade were both inside the eye position field, most
neurons (82%) responded less well; however, when the saccade began
outside and then entered the eye position field, the neurons responded
vigorously. Therefore these neurons did not encode the static position
of the eyes so much as the dynamic arrival of the eyes at the preferred
site. This emphasis on a change in status, rather than on the steady
state, may be a fundamental property of sensory processing. For
example, in the visual system, neurons are most sensitive to the
borders between two luminances or colors rather than to a region of
uniform luminance or color (Hubel 1988). In
view of the current data, the same emphasis on encoding a change in
status appears to apply to the representation of eye position. One
possible function of the eye position information in V6A is discussed
in the final section.
Where is the "where" pathway?
In 1982, Ungerleider and Mishkin proposed that extrastriate visual
cortex is organized in two processing streams, a ventral stream that
processes the identity of objects and a dorsal stream that processes
the spatial locations of objects. Subsequent work has shown that, in
the ventral stream, neuronal responses to shape, color, and texture
increase in complexity along a sequence of interconnected areas
including V1, V2, V4, and IT (for review see Desimone et al.
1985; Gross et al. 1993
). The dorsal stream, however, was more difficult to specify. Neuronal responses to visual
motion increase in complexity along a sequence of areas including V1,
V2, MT, MST, and STP (for review see Graziano et al.
1994a
). However, there is little evidence that these areas are
involved in processing spatial location per se. Indeed lesions to MT
seem to affect the processing of motion rather than spatial location
(Newsome and Pare 1988
). Where is the where system, that is, what are the areas that process spatial location, and are they
organized in a hierarchical fashion?
Areas that process space must carry more than just visual information.
They must also carry information about the position of the eyes and
other body parts to reconstruct the location of visual stimuli with
respect to the body. Because of its combination of visual and
proprioceptive information, parietal area 7a is considered an important
processing station for space (Andersen 1987). Recently
several other areas, including V3a, PO, and V6A, were found to carry
similar spatial information (Galletti et al. 1993
, 1995
,
1996
). Therefore we suggest that these areas may be part of the
missing spatial processing stream and that area V6A, with its high
proportion of eye-position sensitive neurons, may serve as one source
of the eye-position information that is critical for spatial processing
in other parietal areas.
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ACKNOWLEDGMENTS |
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This work was supported by Human Frontier Science Program Grant LT-716/94, the Uehara Memorial Foundation, and the National Eye Institute Grant EY-11347.
Present address of K. Nakamua: Primate Research Institute, Kyoto University, Inuyama, Aichi 484, Japan.
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FOOTNOTES |
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Address for reprint requests: M. Graziano, Dept. of Psychology, Green Hall, Princeton University, Princeton, NJ 08544.
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 19 March 1998; accepted in final form 11 January 1999.
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REFERENCES |
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