1Laboratory of Sensorimotor Research, National Eye Institute, Bethesda, Maryland 20892; 2Department of Physics, The American University, Washington 20016; and 3Department of Neurology, Georgetown University School of Medicine, Washington, DC 20007
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ABSTRACT |
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Umeno, Marc M. and Michael E. Goldberg. Spatial Processing in the Monkey Frontal Eye Field. II. Memory Responses. J. Neurophysiol. 86: 2344-2352, 2001. Monkeys and humans can easily make accurate saccades to stimuli that appear and disappear before an intervening saccade to a different location. We used the flashed-stimulus task to study the memory processes that enable this behavior, and we found two different kinds of memory responses under these conditions. In the short-term spatial memory response, the monkey fixated, a stimulus appeared for 50 ms outside the neuron's receptive field, and from 200 to 1,000 ms later the monkey made a saccade that brought the receptive field onto the spatial location of the vanished stimulus. Twenty-eight of 48 visuomovement cells and 21/32 visual cells responded significantly under these circumstances even though they did not discharge when the monkey made the same saccade without the stimulus present or when the stimulus appeared and the monkey did not make a saccade that brought its spatial location into the receptive field. Response latencies ranged from 48 ms before the beginning of the saccade (predictive responses) to 272 ms after the beginning of the saccade. After the monkey made a series of 16 saccades that brought a stimulus into the receptive field, 21 neurons demonstrated a longer term, intertrial memory response: they discharged even on trials in which no stimulus appeared at all. This intertrial memory response was usually much weaker than the within-trial memory response, and it often lasted for over 20 trials. We suggest that the frontal eye field maintains a spatially accurate representation of the visual world that is not dependent on constant or continuous visual stimulation, and can last for several minutes.
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INTRODUCTION |
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Monkeys and humans can easily
make eye movements to remembered targets (Hikosaka and Wurtz
1983). They can do it even in a double-step task where another
saccade intervenes between the disappearance of the target that evokes
the saccade and the eye movement necessary to acquire it
(Hallett and Lightstone 1976
; Mays and Sparks
1980
). Neurons in the frontal eye field (Bruce and
Goldberg 1985
), prefrontal cortex (Funahashi et al.
1989
), and lateral intraparietal area (LIP) (Barash et
al. 1991
; Goldberg et al. 1990
) show evidence of
a visual-memory signal, responding in a tonic manner to briefly flashed
targets. This activity occurs even in a fixation task in which monkeys
do not make a saccade to the stimulus that evokes the response
(Colby et al. 1996
). Neurons in the frontal eye field
(Goldberg and Bruce 1990
), superior colliculus
(Mays and Sparks 1980
), and LIP (Barash et al.
1991
; Goldberg et al. 1990
) all discharge
appropriately before saccades in a double-step task. They discharge
before saccades into their movement fields even though there is a
dissonance between the retinal location of the stimulus and the saccade
necessary to acquire the target.
Recent experiments have suggested that such spatially accurate
presaccadic activity can occur because some neurons in these areas are
capable of two different kinds of nonclassical visual responses. The
first is a predictive visual response: neurons in LIP (Duhamel
et al. 1992), the superior colliculus (Walker et al.
1995
), and the frontal eye field (Umeno and Goldberg
1997
) respond to targets that will be brought into their
receptive fields by an impending saccade, even if the stimulus never
appears in their visual receptive fields as determined in a fixation
task. The predictive visual response occurs before the saccade. If the stimulus remains illuminated after the saccade moves it onto the retinal receptive field, there is a reafferent response that reinforces the initial predictive response.
The majority of neurons in LIP only discharge after the saccade brings
a stimulus into the receptive field. The simple assumption is that this
postsaccadic response is merely a reafferent response. However, in LIP,
for many neurons, there is a visual-memory response that contributes to
postsaccadic activity. If a stimulus flashes at the spatial location
that will enter the receptive field as a result of a saccade but
disappears before the saccade, the neurons discharge after the saccade
in response to the flashed target (Duhamel et al. 1992)
(see Fig. 1 for a diagram of this experiment). Although the response
occurs after the saccade, it is a response to a stimulus that appeared
only before the saccade in a retinal location outside the receptive
field as determined in a fixation task. If the only component of the
postsaccadic response was visual reafference, the cell would be
expected to remain silent because the saccade does not bring the
stimulus into the receptive field. The stimulus vanished before the
saccade began. If the additional postsaccadic signal were a
postsaccadic movement response, one would expect to see it after every
saccade regardless of whether or not a stimulus had recently flashed.
Instead LIP neurons exhibiting spatially accurate memory responses
discharge after only those saccades that bring the spatial location of
a recently vanished stimulus onto the receptive field. Similar
spatially accurate visual memory responses were demonstrated in the
intermediate gray layers of the monkey superior colliculus
(Walker et al. 1995
).
In these experiments, we asked if a similar memory response was present
in the frontal eye field of the monkey. We found two different kinds of
memory responses: a short-term within-trial memory response that
resembles that seen in LIP and the superior colliculus and a
longer-term intertrial memory response that has not been previously
described. A preliminary report of these results has been presented in
abstract form (Umeno and Goldberg 1998).
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METHODS |
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Surgical and physiological methods were described in a recent
report (Umeno and Goldberg 1997). All animal protocols
were approved by the Animal Care and Use Committee of the National Eye
Institute and certified to be in compliance with the Public Health
Service Guide for the Care and Use of Laboratory Animals.
Behavioral methods
Monkeys were trained on a number of baseline tasks all of which
have been described previously. Cells were characterized first using
either visually guided or the memory-guided delayed saccade tasks
(Hikosaka and Wurtz 1983). In the latter, the monkey was required to hold its gaze on a fixation point, and during this fixation, a peripheral visual stimulus (a red light-emitting diode) appeared in the spatial position of the receptive field; it was extinguished after a fixed period of time, usually 50 ms. When the
fixation point disappeared, the monkey made a saccade to the location
of the now-vanished visual stimulus. If the monkey made a saccade
within a window of 25% of the desired saccade amplitude around the
target location, the light reappeared after the saccade, and the monkey
was rewarded for holding fixation at that location for 100 ms. This
task enabled us to characterize presaccadic frontal eye field neurons
according to the classification of (Bruce and Goldberg
1985
) as visual, visuomovement, or movement. Visual cells responded in a time-locked manner to the onset of the visual stimulus in their receptive fields and were silent during the saccade. Movement
cells were silent during the stimulus presentation and responded just
before saccades to their movement fields. Visuomovement cells responded
to the visual stimulus and before the saccade.
We then studied presaccadic neurons in two tasks designed to show the
effects of saccades on the neuron's receptive field: the flashed
stimulus task and the continuous stimulus task (Fig. 1). In both tasks, the monkey held its
gaze on a fixation light, FP1. In the flashed stimulus task, a visual
stimulus (STIM) appeared for 50 ms at a location outside of the
neuron's receptive field. We call the receptive field location during
this first fixation the current receptive field (CRF). After a
pseudorandom interval between 800 and 1,000 ms, FP1 disappeared, and a
saccade target, FP2, appeared at a location chosen so that when the
monkey made a saccade to it, the eye movement brought the spatial
location of the now-vanished STIM into the neuron's receptive field.
We call the spatial location that will be brought into the receptive field the future receptive field (FRF) because that spatial location will occupy the receptive field of the neuron after the saccade. The
FRF stimulus was always located so that the cell never responded to it
either when it appeared during fixation or before the saccade when the
monkey made a memory-guided saccade directly to it. The monkey then had
to make a second saccade to FP3 after another 500 ms. This second
saccade was never made to the location of STIM or to any part of the
neuron's receptive field. For some, but not all, receptive field
locations the second saccade removed STIM from the neuron's receptive
field. The continuous stimulus task was identical to the flashed
stimulus task except that STIM remained illuminated for the duration of
the trial (Umeno and Goldberg 1997).
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We used two types of control experiments for activity evoked in the flashed stimulus task. The no-stimulus control task was a saccade task in which the monkey made a saccade from FP1 to FP2 but no stimulus appeared while the monkey fixated; in an alternate version, a stimulus appeared on the screen but it was in neither the current nor the FRF and never entered the neuron's receptive field during the trial. In the no-saccade control task, the monkey fixated and the stimulus appeared at STIM, but the monkey made no saccade. In an alternate version of this task (the null saccade control), the monkey made a saccade that did not move the spatial location of STIM into the receptive field. For experiments in which the saccade signal appeared more than 400 ms after the appearance of STIM and at several different times, we did not always run the no-saccade control because there was no consistent response to the stimulus at these long latencies. For most of these experiments, we ran the trial types in blocks with the no-saccade and no-stimulus tasks performed first and followed by the flashed stimulus task and continuous stimulus task. For some experiments, all four tasks were run in a randomly interleaved fashion after they had first been run in blocks.
Data analysis methods
We determined each neuron's visual latencies and discharge
frequency off-line, using a series of data analysis programs written in
C running on a Silicon Graphics workstation. We rejected trials in
which the monkey failed to earn a reward. We smoothed the eye position
traces using a finite impulse response filter with a low-pass roll-off
of 3 dB at 53.7 Hz. To determine the beginning and end of saccades, we
digitally differentiated eye position traces using a differentiating
finite impulse response filter with a 3-dB roll-off at 211.9 Hz, and
computed when the velocity rose above a value, usually 50°/s. We
chose this relatively high value to reject microsaccades and fixation
breaks automatically. We used 15°/s as the value to determine the end
of the saccade. We verified the computer's estimate of saccade
beginning and end by visual inspection of the traces. We found that we
rarely had to adjust the computer's estimate of saccade beginning,
although occasionally the computer would pick up a saccade before the
fixation point went out, in which case we found the next saccade, or
the monkey made too slow a saccade and the computer failed to identify any, in which case we lowered the velocity criteria for that
trial only. We computed rasters, histograms, cumulative histograms, and
spike density probability functions (Richmond et al.
1987) synchronized on stimulus onsets and offsets and saccade
beginnings and ends from the accepted trials, using a binwidth of 2 ms.
We calculated spike discharge frequency as the average in the 100 ms
following the onset of the burst. We defined the beginning of the burst
as the first inflection point in the cumulative histogram after the
appearance of the stimulus or the signal to make the saccade. To find
this point, we computed the cumulative histogram by adding all of the
spikes in a given 2- or 4-ms bin and then differentiating it using the
same finite impulse response filter that we used for the eye position
trace. We defined the beginning of the burst as 10 ms before the
differentiated cumulative histogram value was greater than a value
usually set at 12.5 spikes/s/trial. The cursor placement was verified
by inspection to ensure that the program did not pick out a burst that
began before the fixation point went out.
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RESULTS |
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The data set in this report is the same as that in the previous
report (Umeno and Goldberg 1997). We recorded from three
hemispheres of two awake behaving Rhesus monkeys and used the delayed
or visually guided saccade tasks to classify presaccadic neurons into
visual (32 cells) and visuomovement (48 cells). We found two different sorts of visual memory
a short-term spatial memory that occurred in a
single trial and a longer-term memory that lasted for as long
as 30 trials.
Short-term spatial memory
We tested the responses of the 80 visually responsive neurons
using the flashed stimulus task. This task exposed the neurons to a
stimulus that flashed only in the FRF, the spatial location that would
lie in the neuron's receptive field after the saccade. The stimulus
never appeared in the visual receptive field of the neuron as
determined in the delayed saccade task. A majority [61% (49/80)] of
the visually responsive cells responded in the flashed stimulus task,
i.e., the cell responded around the time of the saccade to a stimulus
that appeared only in the FRF. We did not test movement cells in the
flashed stimulus paradigm: these cells never responded to the stimulus
in the continuous stimulus task before or after the saccade because the
monkey never made a saccade to the stimulus (Umeno and Goldberg
1997). Given that there was no response to a sustained
stimulus, it was extremely unlikely that the cells, which had no visual
response even to a stimulus in their movement field, would respond to a
transient, irrelevant stimulus outside their movement fields.
VISUOMOVEMENT NEURONS. We studied 48 visuomovement cells, of which 28 responded in the flashed stimulus task (58%). Visuomovement cells responded to the appearance of the stimulus in a saccade task and also discharged before the beginning of the saccade (Fig. 2A). The neuron illustrated did not show a predictive effect in the continuous stimulus task: the neuron discharged only after the saccade, with latency comparable to the latency of the neuron's response to the appearance of the visual stimulus (the on-response; Fig. 2B). Note that the STIM did not appear in any part of the current receptive field: the latency of the response was prolonged relative to the absolute appearance of the stimulus, and the response was best synchronized to the saccade and not to the stimulus appearance. If the STIM had been capable of driving the cell itself, one would have expected it to do so with latency similar to its response to the stimulus when it appeared in the current receptive field (Fig. 2A). Nonetheless, the neuron did respond in the flashed stimulus task: when the stimulus appeared and disappeared in the FRF, the neuron discharged after the saccade that brought the spatial location of the vanished stimulus into the receptive field (Fig. 2C). The activity was not a response to the saccade alone: when the monkey made the identical saccade in the no-stimulus control task where there was no stimulus flashed in the future receptive, the cell did not discharge (Fig. 3A). The activity was not a response to the stimulus flashed at that location: When the monkey made a saccade that moved the spatial location of the same flashed stimulus from one location outside the receptive field to another location outside the receptive field, there was no discharge (Fig. 3B). The monkey was unlikely to be preparing a saccade to the stimulus in the FRF because the monkey always had to make a second saccade to another fixation point in the interval after the first saccade. The computer randomly interleaved the trials illustrated in Figs. 2 and 3. We define this response to a stimulus that only appeared in the current receptive field but whose spatial location lies in the FRF as a short-term spatial memory response.
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VISUAL NEURONS. Sixty-six percent (21/32) of the visual cells exhibited short-term spatial memory responses (Fig. 6). The neuron illustrated fired 78 ms after a visual stimulus appeared its receptive field (Fig. 6A, left) and had no burst before the saccade to the location of that stimulus (Fig. 6A, right). The cell responded at the time of the saccade in the flashed stimulus task (Fig. 6B, right) but gave no response to the appearance of the stimulus in the FRF (Fig. 6B, left). Because this cell discharged before the beginning of the saccade in the continuous stimulus task, it also had a predictive response in the continuous stimulus task (not shown). The cell also did not discharge in association with the identical saccade when saccade brought no stimulus into the receptive field (Fig. 6C).
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SAMPLE POPULATION CHARACTERISTICS.
There was a continuous distribution of latencies from saccade onset,
ranging from 48 to 272 ms (Fig. 7). The
amplitude of the short-term spatial memory response was almost
inevitably less than the visual on response as measured in the delayed
saccade task (Fig. 8).
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Intertrial spatial memory
Short-term spatial memory responses occur within a single trial.
We used the interleaved experimental paradigm to demonstrate effects
between trials. We first ran the no-saccade and no-stimulus control
experiments in blocks and then studied the response of the neuron in
the flashed and continuous stimulus paradigms, also run in blocks. For
60 visually responsive frontal eye field neurons, we then randomly
interleaved trials of all four sorts. At this point, the monkey had
already become accustomed to the stimuli shown in the task. Immediately
before the interleaved paradigm, the monkey had done a block of flashed
or continuous stimulus trials in which a stimulus or the spatial
location of a recently flashed stimulus had been brought into the
receptive field by a saccade. None of the cells studied had responded
in either the no-stimulus or the no-saccade control tasks.
Surprisingly, 21 (35%) of these cells, which had previously been
silent during the initial no-stimulus control task when it was
performed before the flashed or continuous stimulus tasks, now
responded during the no-stimulus control task when it was interleaved
with continuous stimulus trial. A visuomovement cell that demonstrates
this effect is illustrated in Figs. 9 and
10. Note that the cell had
a significant anticipatory response (Bruce and Goldberg
1985) (Fig. 9A): it responded after the saccade to
the fixation point but before the stimulus appeared; this anticipatory
response was less than the visual on response. The cell illustrated had
both a visual (Fig. 9B) and movement response (Fig.
9C) during the delayed saccade task. When the monkey
performed the delayed saccade task in a block of trials, with the
stimulus always in the same place, the cell began to discharge after
the monkey had achieved fixation but before the saccade target appeared
on the screen. When the monkey performed the no-stimulus control task
before any continuous-stimulus or flashed-stimulus trials, the cell was
silent (Fig. 10A). The cell exhibited a marked predictive
response during the continuous stimulus task, discharging before the
identical saccade when that saccade would bring the stimulus into the
receptive field (Fig. 10B). We then randomly interleaved
no-stimulus trials and stimulus trials, with the monkey always making
the same saccade. When we presented stimuli in the cell's FRF during
some of the trials, the cell registered a brisk predictive response
(Fig. 10C), which was then reinforced by the reafferent
response to the stimulus in the receptive field after the saccade.
Surprisingly, even though previously the cell did not discharge during
the saccade control task when that task had been run before any
continuous stimulus trials, the same saccade with no stimulus in the
FRF now elicited a significant response, differing from the response in
the continuous stimulus task only in latency (Fig. 10D). We
interpreted this response as an intertrial memory response: the cell
responded as if the stimulus, present on the majority of recent trials,
were still present on the current trial.
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The intertrial memory response often took a long time to disappear, as long as 30 trials (roughly 1.5 min). Figure 11 shows the forgetting curves for two cells with intense intertrial memory activity.
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Thirty-five percent (21/60) of the neurons had intertrial memory activity, i.e., their activity in the no-stimulus interleaved task was significantly greater (P < 0.05 by t-test) than the background activity measured in one of the control tasks performed before any flashed or continuous stimulus trials had occurred (Fig. 12). For all cells, the intertrial memory response was less than the visual on-response. Unlike the short-term memory responses, no intertrial memory response began before the beginning of the saccade (Fig. 13). This was true even for neurons that demonstrated predictive responses in the continuous stimulus task.
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TONIC RESPONSES. Of the 80 visually responsive cells examined, 20 discharged longer than the stimulus duration (300 ms) in the delayed saccade task. Every one of these cells had at least one of a short-term memory response, intertrial memory response or a predictive response.
COMBINATIONS OF NONCLASSICAL VISUAL RESPONSES. Sixty-two (78%) of the visually responsive cells tested had at least one kind of nonclassical visual response (predictive, short-term spatial memory, intertrial spatial memory responses) demonstrated in the flashed stimulus or continuous stimulus task. Table 1 shows the different combinations of these effects found in this population. Note that the most common response type to be found alone was the short-term memory response. The table only included those cells for which all three types of response were tested.
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DISCUSSION |
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In these experiments, we have demonstrated two different forms of
visuospatial memory in the monkey frontal eye field: a within-trial short-term spatial memory response and a longer-term, intertrial memory
response. The within-trial memory response resembles those demonstrated
in the monkey lateral intraparietal area (LIP) (Duhamel et al.
1992) and superior colliculus (Walker et al.
1995
). In the course of these experiments, however, we found a
rather unexpected effect: a low-frequency discharge that occurred when
the monkey revisited a fixation location where, for a block of trials
in the recent past, a stimulus had appeared in the receptive field of
the neuron. This intertrial spatial memory effect required a number of
trials to disappear. We will discuss these phenomena in the context of
their relationship to visual processing and to their resemblance to
other demonstrations of memory in the monkey brain.
Short-term spatial memory as a visual phenomenon
Visual memory has been demonstrated in the frontal eye fields
(Bruce and Goldberg 1985) and also in a number of other
areas of the monkey brain, including the prefrontal (Funahashi
et al. 1989
; Fuster and Alexander 1971
),
inferotemporal (Fuster and Jervey 1981
), and parietal
cortices (Colby et al. 1996
; Gnadt and Andersen 1988
) and the substantia nigra pars reticulata (Hikosaka
and Wurtz 1983
). In these areas, the memory is manifest by a
tonic, continuing response to a stimulus that appeared transiently
during a fixation task. Although in some of these areas the activity
was first demonstrated in the context of a delayed saccade task, in the
frontal eye fields (Bruce and Goldberg 1985
) and in LIP
(Colby et al. 1996
), the saccade is not necessary for
the tonic visual response. In these experiments, we demonstrated a new
property of the visual memory response in the frontal eye field. The
stimulus need not appear in the receptive field of the neuron as
determined in a simple fixation or delayed-saccade task. Instead,
neurons with a visual response can respond after a saccade to a
stimulus that appeared briefly before the saccade when that saccade
brings the spatial location of the vanished stimulus into the visual
receptive field of the neuron. This effect depends not on the
trajectory of the saccade, nor on the absolute spatial location of the
target, but instead on the combination of the two: the saccade must
bring the spatial location of the vanished stimulus into the receptive field of the neuron. This effect resembles the predictive visual response described previously (Umeno and Goldberg 1997
),
but it can occur in neurons that do not demonstrate a predictive
response, neurons that discharge after but not before a saccade brings
a stimulus into their receptive field.
Because the frontal eye field is primarily dedicated to the generation
of purposive eye movements, one could argue that the spatial memory is
actually a premotor discharge signaling a saccade that is canceled
elsewhere in the brain. Such cancellation could occur at the level of
the fixation neurons in the superior colliculus (Munoz and Wurtz
1993) or the omnipause neurons in the dorsal raphé
(Buttner-Ennever et al. 1988
). However, we never saw a predictive response on a movement neuron (Umeno and Goldberg
1997
); these neurons require that the monkey actually make the
saccade, and it would be unlikely for them to respond to a transient
stimulus when they failed to response to the onset of a more sustained stimulus. In addition, the task was designed so that the monkey predictably made a saccade to a stimulus outside the receptive field
immediately after the saccade that evoked the memory response. It would
be difficult to argue that the response was due to an active planning
of the saccade to the spatial location of the target when the monkey
could predict that its next saccade would be to a different target.
Therefore the within-trial memory response must be a property of the
visual processing of the frontal eye field or its afferents. Similar
within-trial memory responses have been demonstrated in LIP, an area
with a strong reciprocal projection to the frontal eye field.
The stimuli with which we demonstrated both the short-term and
intertrial responses were irrelevant to the monkey's task, and it is
natural to assume that the stimuli were therefore irrelevant to the
monkey. This may not be the case. Flashed stimuli are inevitably salient. Neurons in LIP respond far more intensely when a saccade brings recently flashed irrelevant stimuli onto the receptive field of
a neuron than they do when the same saccade brings the same stimulus
onto the receptive field when it has been stable in the environment
(Gottlieb et al. 1998; Kusunoki et al.
2000
). Because LIP has a strong projection to the frontal eye
field, it would not be surprising if the short-term response resulted from the salience of the task-irrelevant stimulus. The maintenance of
the memory response in the intertrial memory phenomenon may also have
to do with the salience of the stimuli. The visual environment of the
monkeys in these experiments consisted only of three dots in a sea of
darkness rather than the complex visual environment of everyday life.
It could be that a task-irrelevant stimulus is not irrelevant to the
monkey when it is one of only three stimuli that the monkey ever sees.
Certainly the response to a possible saccade target in the superior
colliculus varies inversely with the number of possible stimuli
(Basso and Wurtz 1998
). Similarly, the responsiveness of
visual neurons to stable stimuli in a natural environment brought into
their receptive fields by saccades is marginal (Burman and
Segraves 1994
). If one assumes that the role of the visual
mechanism in the frontal eye field is to provide a spatially accurate
map of salient stimuli that are plausible oculomotor targets, then in
the experimental environment that we have used, the irrelevant stimuli
can evoke intertrial and short-term responses because, given the
sparseness of the environment, they cannot help but be salient.
It is important to emphasize that short-term spatial memory is not an explicit spatial representation. The neurons describe the distance and direction of the stimulus from the fovea, i.e., a vector, rather than the absolute spatial location of the stimulus in supraretinal coordinates. As the eyes move, the ensemble of neurons representing a given stimulus moves. This enables the frontal eye field to maintain a spatially accurate representation of possible saccade targets despite a moving eye. The shift of representation, of course, would be expected if the stimulus were still present; in short-term spatial memory the ensemble representing the trace of the stimulus shifts around the time of the saccade even though the stimulus never appeared in the receptive fields of the postsaccadic ensemble.
This short-term spatial memory, although unlikely to be a saccadic signal per se, is immensely useful to the saccadic system. By automatically updating the frontal eye field's representation of the remembered world, the phenomenon facilitates spatially accurate saccades to the spatial locations of stimuli that flashed briefly before intervening saccades without requiring an explicit representation of target position in some supraretinal coordinate system.
The short-term memory resembles the predictive response and may share
some of its underlying neural processing. However, the majority of
neurons with short-term memory responses do not have predictive
responses. The predictive and memory responses can be modeled by
assuming that the visual system has access to a signal describing the
change in eye position (Quaia et al. 1998). In the
predictive response, the change in eye position must be signaled by a
corollary discharge from the oculomotor system because it comes before
the eye actually moves. The change in eye position signal for those
neurons that have short-term memory responses after the saccade could
arise from a proprioceptive signal of the new eye position.
Intertrial memory
The time interval of memory is greater than a visual fixation. The
studies quoted in the preceding text have all demonstrated within-fixation mnemonic responses and not responses that lasted for
longer intervals. In these experiments, however, we have demonstrated that once a spatial location becomes established as associated with a
visual stimulus, activity referable to that stimulus remains for a
number of trials after the stimulus has vanished. Spatial memory
responses have been demonstrated in the hippocampus of the rat
(O'Keefe 1999) and monkey free to move in space
(Eifuku et al. 1995
). These neurons discharge when the
animal occupies a certain place, and the nature of the place can be
established by cues of many modalities. This hippocampal memory can be
considered a cognitive memory for location. The memory that we have
described in these experiments is more likely to be a more specialized
form of memory, a memory for trajectory. Unlike the hippocampal
neurons, which are probably independent of eye position, the frontal
neurons are dependent on the establishment of a vector between eye
fixation and target location. Once the visual location of a target has been established, the presence of that target is no longer necessary for the guidance of eye movements to its spatial location, and monkeys
can performed saccades to the location of a target that appeared only
on previous trials (Bruce and Goldberg 1985
). We suggest
that the intertrial mechanism that we have established can provide the
substrate for the memory that allows the performance of such learned
saccades. Like the predictive visual responses (Umeno and
Goldberg 1997
) and the within-trial memory responses, intertrial memory responses are a property of visual processing. They
are seen on visual and visuomovement neurons and not movement neurons,
and they occur despite the fact that the monkey does not make a saccade
to the spatial location of the vanished stimulus that evokes the response.
The intertrial memory may be responsible for some component of the
anticipatory response. Neurons in the frontal eye field have often have
increased activity before the appearance of the stimulus when the
monkey performs a block of saccade trials (Bruce and Goldberg
1985). Although the original interpretation was that the monkey
was anticipating the appearance of the saccade target, this activity
could actually be an intertrial memory response. We discovered neurons
with intertrial memory that also showed anticipatory responses (Fig.
9).
The three nonclassical visual responses that we have demonstrated in
this and the preceding paper (Umeno and Goldberg 1997) are distributed in a way that suggests that they are generated independently. Clearly many cells with memory responses do not have the
latency advance that is the hallmark of the predictive responses. It is
curious that cells with predictive or intertrial responses do not have
short-term responses but that may be due to an inability to respond to
transient task-irrelevant stimuli.
These results suggest that whenever a monkey achieves a visual fixation, the frontal eye field develops a representation of potential saccade targets based on the animal's recent experience. These targets include present and recently vanished objects, evoked by visual and memory responses. However, this representation of potential saccade targets is far earlier in the saccadic processing chain than the actual decision to make a saccade.
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FOOTNOTES |
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Address for reprint requests: M. E. Goldberg, Laboratory of Sensorimotor Research, National Eye Institute, Bldg. 49, Rm. 2A50, Bethesda, MD 20892-4435 (E-mail: meg{at}lsr.nei.nih.gov).
Received 5 October 2000; accepted in final form 31 July 2001.
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