Download Visual Responses of Pulvinar and Collicular Neurons During Eye

JOURNALOF NEUROPHYSIOLOGY
Vol. 66, No. 2, August 199 1. Printed
in U.S.A.
Visual Responses of Pulvinar and Collicular Neurons
During Eye Movements of Awake, Trained Macaques
DAVID LEE ROBINSON,
JOHN W. McCLURKIN,
CAROLINE
KERTZMAN,
AND
Section on Visual Behavior, Laboratory ofSensorimotor Research, National Eye Institute,
National Institutes of Health, Bethesda, Maryland 20892
SUMMARY
AND
CONCLUSIONS
1. We recorded from single neurons in awake, trained rhesus
monkeys in a lighted environment
and compared responses to
stimulus movement during periods of fixation with those to motion caused by saccadic or pursuit eye movements. Neurons in the
inferior pulvinar (PI), lateral pulvinar (PL), and superior colliculus were tested.
2. Cells in PI and PL respond to stimulus movement over a
wide range of speeds. Some of these cells do not respond to comparable stimulus motion, or discharge only weakly, when it is generated by saccadic or pursuit eye movements. Other neurons respond equivalently to both types of motion. Cells in the superficial
layers of the superior colliculus have similar properties to those in
PI and PL.
3. When tested in the dark to reduce visual stimulation from
the background, cells in PI and PL still do not respond to motion
generated by eye movements. Some of these cells have a suppression of activity after saccadic eye movements made in total darkness. These data suggest that an extraretinal signal suppresses responses to visual stimuli during eye movements.
4. The suppression of responses to stimuli during eye movements is not an absolute effect. Images brighter than 2.0 log units
above background illumination
evoke responses from cells in PI
and PL. The suppression appears stronger in the superior colliculus than in PI and PL.
5. These experiments demonstrate that many cells in PI and PL
have a suppression of their responses to stimuli that cross their
receptive fields during eye movements. These cells are probably
suppressed by an extraretinal signal. Comparable effects are present in the superficial layers of the superior colliculus. These properties in PI and PL may reflect the function of the ascending tectopulvinar system.
INTRODUCTION
Motion can be produced by the movement of visual stimuli in the external environment or it can be generated by
saccadic or smooth pursuit eye movements. Central visual
pathways must distinguish between these two sources of
visual stimulation (von Helmholtz 1925). There are several
contexts in which the brain must know how stimulus motion is produced. First, it is important for perception. Organisms need to know if an object moved or if visual field
motion is derived from eye movements. Second, neural
mechanisms that initiate responses to movement should
not be falsely triggered by image motion that is self induced.
Finally, those parts of the brain that control smooth pursuit
and optokinetic eye movements need to deal differently
with image motion, depending on its origin. Errors in mo-
STEVEN
E. PETERSEN
tion discrimination
would lead to unstable oculomotor
control.
Some have proposed that there is a corollary discharge
from the oculomotor system to the visual system that indicates the presence of reafferent stimulation (von Holst and
Mittelstaedt 1950; Sperry 1950; Teuber 1960). Others suggested purely visual processes or visual masking as mechanisms for eliminating
vision during saccadic eye movements (Campbell and Wurtz 1978; MacKay 1970; Matin et
al. 1972). It seems likely that both types of mechanisms
(visual and extraretinal) contribute to conscious perception, oculomotor control, and other aspects of visual behavior.
Several cortical areas have been investigated to understand visual responsiveness around the time of eye movements. Visual activity during saccadic and smooth pursuit
eye movements has been tested in areas 17, 18, 19, and 7
(Battaglini et al. 1986; Fischer et al. 198 1; Galletti et al.
1984, 1986, 1988; Judge et al. 1980; Sakata et al. 1985;
Wurtz 1969). Each of these regions has varying concentrations of neurons that respond differentially for real and selfinduced stimulus movement. We have shown that cells
in the superior colliculus respond differentially to rapid
stimulus movement (Robinson and Wurtz 1976). In the
present studies we have found that cells in the retinotopitally organized regions of the inferior pulvinar (PI) and lateral pulvinar (PL), which are targets of collicular projections, also respond differentially to stimulus movement
(Benevento and Fallon 1975; Benevento and Standage
1983; Marrocco et al. 1981; Partlow et al. 1977). We hypothesize that an extraretinal signal reduces responses to
stimuli during eye movements. These data suggest that
such processes may originate in the colliculus, be transmitted to PI and PL, and from there influence visual cortex.
Brief reports of these studies have appeared previously
(McClurkin
and Robinson 1987; Robinson and Petersen
1985).
METHODS
Four rhesus monkeys (3 males, 1 female; 4.0-M kg) were used
in these experiments. Initially each was trained to fixate a small
spot of light and to release a bar when the fixation point dimmed
to receive a water reward. After the monkeys had achieved a performance criterion, they were implanted with a cranial pedestal and a
scleral search coil using sterile surgical procedures (Petersen et al.
1985).
For the surgery, each monkey was premeditated
with atropine
sulfate (0.05 mg/kg im) to reduce respiratory tract secretions and
485
486
ROBINSON
with cephalothin sodium (50 mg/kg im) to combat infection. Initial anesthesia was induced with ketamine HC1(4-60 mg/kg im).
After the ketamine, pentobarbital
sodium (20-33 mg/kg) was
given through a transcutaneous catheter inserted into the saphenous vein, and the monkey was placed in a stereotaxic frame.
Heart rate, respiratory rate, and body temperature
were monitored and body temperature was controlled with a heating pad.
After the surgery, the monkey was allowed to recover in an incubator in which the temperature was maintained at 80’F. When the
monkey was alert, it was returned to its home cage. For 2 days
after the surgery, each monkey was administered pentazocine lactate (1 S-3.0 mg/kg im) to relieve any postoperative discomfort.
The monkeys were given food and water ad lib, were checked
daily, and were given prophylactic cephalothin
sodium for 1 wk.
All procedures were conducted under a protocol approved by the
Animal Care and Use Committee of the National Eye Institute
and complied with Public Health Service Policy on the humane
care and use of laboratory animals.
Behavioral
tasks
After the monkeys had fully recovered from the surgery, they
were retrained on the fixation task while their heads were restrained. To train the monkeys to maintain precise fixation, we
monitored
eye position and terminated trials if the eye moved
outside of a computer-generated,
2O-square window surrounding
the fixation point (Fig. IA). Once they were able to fixate correctly,
they were trained to make saccadic eye movements from one stimulus to another on simultaneous termination
of the fixation point
and appearance of a target. They also learned to make smooth
pursuit eye movements by following the slow, continuous movement of the fixation point. Both of these eye movement tasks
required that eye position be maintained within 2’ of the desired
location. In all conditions, the monkey’s task was to detect the
dimming of a target light.
The following conditions were used to assess the response characteristics of cells in relation to several types of stimulus movement. All testing was done binocularly. During repeated fixations,
the visual receptive field was determined with a hand-held ophthalmoscope. Then the speed preference of a cell was measured by
sweeping a stimulus through the receptive field at eight speeds
ranging from 10 to 64O”/s in a pseudorandom
order (Fig. IA). The
stimuli consisted of circles or bars with a luminance of 1.5 log
units above the background of 1 cd/m2. The size, shape, and direction of movement of the stimulus was selected to elicit a consistent
response from the cell. On other blocks of trials the monkey made
pursuit eye movements at 2O”/s or saccadic eye movements to
peripheral targets; both were configured to sweep the cell’s receptive field across a stationary stimulus (Fig. 1B). The stimulus was
the same one used in the speed preference experiments. Stimuli
were selected and positioned to ensure that the visual receptive
field actually crossed them even with slight variations in the trajectory of the eye movement. To measure the strength of observed
effects, we increased the brightness of the stationary stimulus up to
a maximum of 3.1 log units above the intensity of the background.
The pursuit targets traveled a distance of 20’ from the center of
the screen to the periphery, and the saccade targets were presented
at an eccentricity of 20’ in either the horizontal or vertical direction. Finally, the same eye movements were made without a stationary stimulus (Fig. 1C).
The monkeys also were trained to make saccades to remembered targets in total darkness (Hikosaka and Wurtz 1983). In this
paradigm the saccade target was flashed on for 75 ms; after an
interval ranging pseudorandomly
from 50 to 500 ms, the fixation
point was turned off, signalling the monkey to make a saccade to
the place where the target had been. This situation eliminated the
possibility of visual interactions. The monkey was rewarded if its
ET AL.
Moving
Fixation
Light
/-----~~~
Stimulus
(IpI
Receptive
Field
(-j-j-t
Rec~c;~
Fi;ld
Eye Position
Window
1
B
Eye Position
Window#2
Saccade
Target ~~7~~~~~~~~u,us
Fixation
Light
/.
Eye Position
Window
#1
C
1
FIG. 1.
Experimental
conditions.
A: tangent screen in the real stimulus
movement
condition.
The monkey
was required
to fixate a central light,
keeping his eye within the eye position window.
The receptive field of a cell
was plotted by hand and a stimulus
was swept through
it. In the self-induced image motion condition
(R), the monkey
began the trial by fixating
a central spot and then a stationary
stimulus was presented on the tangent
screen. Next, the fixation
point was extinguished,
and simultaneously
a
target was turned on in the periphery:
the monkey
made a saccade to fixate
this target. In the pursuit condition,
after the stationary
stimulus was presented, the fixation point was moved slowly, and the monkey
was required
to follow it, keeping his eye within a window.
In both of these conditions,
the resulting eye movements
swept the receptive field across the stationary
stimulus.
C: no-stimulus
condition.
The monkey
was required
to make
either pursuit or saccadic eye movements
as before, but no receptive-field
stimulus was present.
eye position ended inside a 4’ window
the previously illuminated
target.
surrounding
the location of
Recording locations
Recordings were made from the two retinotopically
organized
regions of the pulvinar [inferior map (PI) and lateral map (PL)]
and the superficial layers of the superior colliculus. The techniques for locating these structures have been described in detail
previously (Petersen et al. 1985). Guide tubes were positioned in
various parts of the maps of each of these structures and several
penetrations were made at each location with tungsten microelectrodes (Crist et al. 1988). We tested a total of 20 guide-tube loca-
REAL AND SELF-INDUCED
tions in PI and PL (6 definitely localizedin PI, 7 unambiguouslyin
PL, and 7 at the vertical meridian betweenPI andPL) and 6 in the
superiorcolliculus. We made an averageof nine penetrationsin
eachguide tube (range:2-19). Collicular penetrationswere continued until we encounteredneuronsthat dischargedbefore eye
movements.Previousresearchindicatesthat suchcellsarelocated
in the intermediatelayers(Wurtz and Goldberg 1972).Wedid not
sampleenoughcells unequivocally located in PI or PL to make
quantitative distinctionsbetweenthem for the propertiesstudied
here. However, at leastthree cellswith any particular qualitative
property were unequivocally located in each map. The bulk of
cellshad fields located in the lower visual quadrant with eccentricities from 0” to 20”. At the sitesof interestingcells,we passed6
PA of anodalcurrent for 30-60 s to makemarking lesions,which
were later located on histological sections.The brains were pre-
OBJECT MOTION
487
paredfor histologicalprocessingafter the animal, under deepbarbiturate anesthesia(250 mg/kg ip), was perfusedwith salinefollowedby formaldehyde.Figure 2 showsa microelectrodelesionin
PI aswell asreconstructionsof a penetration in PI and one in PL.
Response quantijcation
All activity wasaligned on a trigger event that wasspecificfor
eachtask. In the fixation task,the event wasthe start of the stimulus movement. In the saccadetask, the event wasthe moment at
which the eyeleft the 2” window surroundingthe fixation point.
In the pursuit task, the trigger wasthe start ofthe movementofthe
pursuit target. Cell dischargesevoked during pursuit were Iate in
the display, comparedwith other conditions, becauseof the slow
speedof the target. Activity wassummedby replacingeachspike
B
FIG. 2. Reconstruction
of penetrations
into PI and PL. The outline drawing in A shows the path of a penetration into PI
(long, vertical line) with tick marks indicating the locations of 5 recording sites. B: receptive-field sizes and locations for the
neurons studied during the penetration in A. Dashed lines connect the field centers. C: another penetration into PL from
which 6 neurons were studied, the corresponding receptive-field data are in D. E: photomicrograph of section through the
pulvinar showing a penetration marked with an electrolytic lesion. The section was stained with cresyl violet. For the
penetration into PI (A and B), at site 1 multi-unit activity was localized; site 2 was a neuron that responded to real but not
self-induced movement in the light and dark; sites 3 and 4 were cells that responded to all speeds tested; site 5 was a neuron
responding best to low-speed motion. From the penetration into PL (Cand D), site 6 was a multi-unit recording; site 7 was a
cell responding well to all speeds; sites 8 and 10 were cells responding equally well to real and self-induced movement; site 9
was a cell activated by real but not self-induced motion; site 11 was a neuron activated best by low-speed movement. Positive
and negative signs in A and C indicate the upper and lower visual fields, respectively. LGN, lateral geniculate nucleus; MGN,
medial geniculate nucleus; FP, fixation point, thus fovea; PDM, dorsomedial portion of the lateral pulvinar (Petersen et al.
1985); PM, medial pulvinar; BSC, brachium of the superior colliculus; H, hippocampus.
488
ROBINSON
TABLE
Distribution
1.
of response characteristics
Saccade
n
Pulvinar
Superior
colliculus
Neurons
movement
qualitatively
ET AL.
Suppressed
Pursuit
Task
Facilitated
No effect
n
Suppressed
Task
Saccade/Pursuit
Facilitated
No effect
n
Similar
effects
Relations
Different
effects*
77
35
10
32
34
10
8
16
22
9
13
24
18
0
6
29
22
1
6
22
14
8
were considered
to be suppressed or facilitated
if the difference between the response during the fixation condition
and the response in the eye
condition
had a P < 0.05 (t test). *Different
effects were noted when the response with saccadic eye movements
(e.g., response facilitation)
was
different from that with pursuit eye movements
(e.g., response suppression).
peripheral bins (affected neurons) of Fig. 5. For the neurons in
each structure we evaluated the strength and distribution of effects
for the whole population by the use of standard errors (Fig. 5). We
used the following formula to calculate the number of standard
errors of the mean by which the responses differed: (X, - &,)/
(SEf + SE,,), where X, is mean response to stimulus movement
during fixation, X,, is mean response to stimuli during eye movement condition, SE,, is standard error of the mean during eye
movement condition, and SE, is standard error during fixation.
Only cells with P < 0.05 were considered significantly modulated
by eye movements, and positive values indicate that the response
in the fixation condition was greater than in the eye movement
situation; negative values represent the opposite. For examining
the distribution of differential responses, we used a t test that compared one population of neurons against a normal distribution of
data with the same number of neurons and the same standard
deviation.
in each trial with a gaussian kernel having a standard deviation of
8 ms, thereby producing a spike density function for each trial
(Richmond
et al. 1987). These spike density functions were
summed within experiments to obtain the summed responses for
each condition.
Responses were quantified by first setting an analysis window
for each condition. The locations and widths of the analysis windows were adjusted so as to capture the whole response observed
in the summed spike density functions. Examples of window placements are illustrated in Fig. 4. When responses of the same cell in
different tasks were to be compared, the same analysis window
width was used. In the speed series, the widths of the analysis
windows became smaller with increasing speed. In the pursuit eye
movement condition, the width of the analysis window was set to
be the same as that used for stimulus movement of 2O”/s. In the
saccadic eye movement condition, the width of the analysis window was set to be the same as that used with stimulus movement
of 64O”/s. The spikes in each analysis window then were counted,
and the mean, standard deviation, and standard error of the mean
were computed to obtain a response measure that was independent of the width of the analysis window and the number of trials
in each condition. This quantification
utilized actual spike data
contained within the windows rather than the spike density functions.
When comparing the responses of a cell in the fixation and eye
movement conditions, we used a Student’s t test for each neuron.
Only cells for which the difference between the means was significant at the P < 0.05 level were considered modulated. This was the
criterion used for categorizing cells for Table 1 and also the criterion for placing neurons in the center bins (unaffected cells) or the
A
RESULTS
We recorded from a total of 243 cells in the two retinotopically organized areas of the pulvinar (PI and PL)
(Bender 198 1; Petersen et al. 1985) and 7 1 neurons in the
superficial layers of the superior colliculus. Of these neurons, we were able to isolate 83 in PI and PL and 35 in the
superior colliculus long enough to obtain complete quantitative data (Table 1).
B
60
40
LD
P
s
1
1
I
200
I
I
400
I
I
2 =
e
n
1
200
600
DEGREE
S/SEC
P
P
1
1
400
I
1
600
FIG. 3. Speed-tuning
characteristics.
Each graph shows the speed data of a different cell. Each circle represents the mean
response of a cell in spikes/second/trial.
Vertical bars above and below each circle
show 1 SE of the mean. The horizontal
line through
each plot depicts the mean
response
for that cell across all speeds
tested. A: responses of a broadly tuned cell.
B: cell tuned to low speeds. C: cell tuned to
intermediate
speeds. D: cell tuned to high
speeds.
FIG. 4.
Responses to stimulus movement.
Data in A and B
illustrate
the responses of 2 cells recorded
in PL during fixation and saccade tasks. Left histogram-raster pair: response to
stimulus
movement
during fixation
(the circle and arrow depicting the stimulus and direction of motion).
Stimulus speed
was 640’1s. Right histogram-raster pair: activity with saccadic
eye movements.
Eye movement
traces from 20” saccades are
above the histogram,
on which it was aligned. The cell in A
responded
well to real but not to self-induced
motion. The cell
in B responded
well to real stimulus movement
and better to
stimulation
generated
during eye movements.
Spike density
functions
were calculated
only from the trials shown in the
raster. The solid vertical line at the left of each raster-histogram pair indicates the beginning
of the stimulus or eye movement, and its height indicates the same scale for the same cell.
The pair of dashed lines in each set of data illustrates the placement of the analysis windows (see METHODS).
Each horizontal
row in the rasters represents a single trial and each dot corresponds to a single action potential.
This data format will be
used in subsequent
figures.
#I56
t
200 MSEC
I
SACCADE
40
c
PULVINAR
PURSUIT
r
A
20 B
l-l
20 -
IO
20 -C
20-D
SUPERIOR
coLLlcuLus I0
FIG. 5.
Comparison
of response differences.
Left: graphs come from expenments
comparing
rapid stimulus movement
during fixation with motion during saccadic eye movements.
Right: data compare responses to image motion of 2O”/s during
fixation
and that induced with smooth pursuit eye movements.
Each row of graphs comes from data collected
from a
different
structure.
Vertical axis indicates the number of neurons with a certain relationship
between real and self-induced
movement.
Center column in each graph includes the cells for which responses in the 2 stimulus movement
conditions
did
not reach the criterion
of significance
at the P < 0.05 level (t test). The first column to the right shows the number of neurons
for which the responses to motion
during fixation
were significantly
different
and between
1 and 3 SE greater than the
responses to motion with eye movements.
The column to the far right represents those cells for which the responses differed
by >3 SE. For the columns to the left of center, with negative values, responses to eye movement
were significantly
greater
than to motion during fixation (t test). See METHODS
for the procedures
and formula
that were used for calculating
standard
error differences.
489
490
ROBINSON
ET
AL.
Self-induced image motion-pulvinar
I
i
400 MSEC
B
%+
360
t
200 MSEC
I
FIG. 6. Similarity
of responses in pursuit and saccade conditions.
A:
data illustrate the responses of a cell in PI to real movements
at 2O”/s and
self-induced
motion in the pursuit condition
at 2O”/s. B: responses of the
same cell to real and self-induced
movement
in the saccade condition
(64O”/s stimulus and 20” eye movement).
In A, the triggers are the start of
the stimulus movement
or pursuit movement
and the response is delayed.
The vertical scales in A are the same even though the number
of trials
differs. Note that the time scales are very different
for A and B.
Responses to stimulus movement duringfixation-pulvinar
We first measured the speed tuning of the neurons in our
sample. Stimuli were swept across the receptive fields of
neurons at each of eight speeds ranging from 10 to 64O”/s
while the monkeys fixated. The mean response to the eight
speeds was computed for each cell, and the responses for the
individual speeds were compared with this mean.
Cells were classified as being broadly tuned to all speeds
or more narrowly tuned to low, intermediate,
or high
speeds. Broadly tuned cells were those in which discharges
to each of the test speeds were within 1 SE of the mean
response. Even those neurons that responded best to some
speeds still discharged at all speeds. Low-speed cells responded to lower speeds 2 1 SE greater than the mean and
to high speeds 2 1 SE less than the mean. Comparable criteria were used for intermediate- and high-speed cells. Examples of four types of speed tuning are illustrated in Fig. 3.
Overall, we found far more broadly tuned than selectively
tuned cells (x2 = 77.48, df = 3, P < 0.001). In PI and PL,
63% (52/83) were broadly tuned whereas 9% (S/83) were
tuned to low speeds, 11% (9/83) to intermediate speeds, and
17% (14/83) to high speeds. We conclude from these data
that cells in PI and PL respond over a very wide range of
stimulus speeds and have marginal selectivity for speed.
After demonstrating that cells in PI and PL respond to
real image movement during periods of fixation, we tested
whether the same cells responded to comparable motion
when it was produced by eye movements. Neurons were
considered to be able to distinguish real from self-induced
movement if their responses in the saccade condition differed from their responses in the fixation condition at least
at P < 0.05 (see METHODS).
The responses of 77 neurons
from PI and PL were examined quantitatively,
and some
gave smaller responses (Fig. 4A), whereas others gave larger
responses (Fig. 4B) in the saccade condition (Table 1). Unequivocal examples of these properties were observed in
penetrations in PI and also in penetrations in PL. Thus
some neurons in PI and PL responded differently to image
movement, depending on how the motion was generated.
These experiments confirm our preliminary observations
(Robinson and Petersen 1985). From our present sample
we found no other property that correlated with the type of
response to eye movements (suppression or facilitation).
Figure 5A shows the distribution of differential responses in
the two stimulus movement conditions. There is a collection of neurons that respond better to real than self-induced
motion (positive standard error values), and this significantly shifts the mean to the right (t = 3.23, df = 76, P <
0.002) when the population is compared with a normal distribution with the same number of samples and the same
standard deviation. For this statistical analysis we used the
actual number of standard errors rather than the binned
groupings in Fig. 5. It is clear from such an analysis that the
retinotopically organized areas of the PI and PL, when considered as a summed, whole population, respond better to
6
I
200 MSEC
FIG. 7. Responses of a collicular
neuron to different
forms of stimulus
motion.
Left: response of the collicular
cell to rapid stimulus
movement
during periods of fixation.
Right: complete
lack of response to the same
stimulus during saccadic eye movements.
REAL
AND
t
SELF-INDUCED
4
400 MSEC
OBJECT
MOTION
491
Superior colliculus
Having demonstrated this differential activity for cells in
PI and PL, we wished to know if such properties were present in another subcortical visual relay structure. We conducted comparable tests of speed selectivity on cells in the
superficial layers of the superior colliculus. In the superior
colliculus, 46% (16/35) of the neurons were broadly tuned
whereas 29% (10/35) were tuned to low speeds, 11% (4/35)
to intermediate
speeds, and 14% (5/35) to high speeds.
These distributions of tuning were not significantly different from those found in PI and PL.
We also studied 24 neurons in the superior colliculus in
the saccade and pursuit conditions. Some collicular neurons gave smaller responses in the saccade condition than
during fixation (Figs. 5A and 7); this is similar to findings
reported by Robinson and Wurtz (1976). The number of
LIGHT
216
t
200 MSEC
FIG. 8. Activity
of collicular
cell with pursuit and saccadic
ments. A: cell responded
clearly to a stimulus
moved through
receptive
field at 2O”/s during periods of fixation
(left). The
sponded when the same stimulus was moved through
the field
pursuit eye movements
(right). B: the same cell also discharged
movement
at 64O”/s during fixations (left) but did not respond
motion was generated by saccadic eye movements
(right).
1
eye movethe visual
cell also reby smooth
to stimulus
when such
stimulus movement during fixation than to stimulus movement generated by saccadic eye movements.
Next we were interested in knowing whether cells in PI
and PL were also modulated during smooth pursuit eye
movements. We tested 34 cells in PI and PL, and some
neurons had reduced responses in the pursuit condition
(Fig. 6A, Table 1). Unambiguous examples of this characteristic were found in both retinotopically
organized areas
of the PI and PL. The responses occur later in the data
displays because the speeds used were much slower than
with saccadic eye movements. Some of these same cells also
had reduced responses when tested in the saccade condition
(Fig. 6B). Of the cells with response reduction during
smooth pursuit, six failed to respond at all to the self-induced movement. Response enhancement during pursuit
was also observed as was equivalent responding in both
conditions. Figure 5B shows the distribution of differential
responding in these two conditions, fixation and pursuit.
There is no significant deviation of the mean from a normal
distribution, and this suggests that PI and PL, when taken
as a whole, summed population, do not distinguish between these two types of slow movement. Table 1 shows the
distribution of response characteristics with saccadic and
pursuit eve movements.
LIGHT
RY499
FIG. 9.
-
200 MSEC
Evidence of an extraretinal
input. Response of a neuron from
PI to real movement
(top).Response to self-induced motion in the light
(center) and the dark (bottom).
This cell failed to respond to self-induced
movement
even when visual inputs were drasticallv
reduced.
492
ROBINSON
cells and the strength of their effect produced a very significant shift in the mean of the population (t = 5.7 1, df = 23,
P 4 0.001) (Fig. 5C). PI and PL and the superior colliculus
have activity that shifts the means of their pooled data toward a differentiation between real and self-induced movement. The superior colliculus population signal is strongly
biased toward responses to real stimulus movement during
fixation; the population signal from PI and PL is also biased
but not as strongly as is the colliculus. Figure 5 also illustrates that the deviation of the mean for pursuit is significant for the superior colliculus (t = 4.7, df = 28, P 4 0.001)
but not for PI and PL.
Of 22 collicular cells tested in both saccadic and pursuit
eye movement conditions, one had equal responses to real
and self-induced movement in both conditions. The responses of 13 cells were suppressed in both pursuit and
saccade conditions. Two cells showed a facilitated response
in the pursuit condition only, whereas six cells had reduced
responses in the saccade condition only. An example of this
latter characteristic is illustrated in Fig. 8. This cell responded briskly to slow image movement, whether it was
generated externally during fixation (Fig. 8A, left) or by
smooth pursuit movements (Fig. 8A, right). The same neuron also responded to rapid image movement during fixation (Fig. 8B, left) but not when produced by saccadic eye
movements (Fig. 8B, right). Table 1 shows that some superior collicular cells responded qualitatively
differently in
the two eye movement situations whereas others had similar responses.
The type of response to self-induced movement did not
depend on speed tuning. This was true for PI, PL, and the
superior colliculus.
We conclude from these data that the responses of many
cells in PI and PL and the superior colliculus are modulated
with eye movements. The strength of the population response is greatest in the superior colliculus and significant
but less intense in PI and PL (Fig. 5).
A
B
LIGHT
ET AL.
Source of difirences
movement
between real and selj?nduced
There are at least two mechanisms that could alter the
response of cells to visual stimuli during eye movements.
One process would use visual interactions with images in
the surround of the visual receptive field. The other mechanism is an extraretinal signal, a nonvisual input to these
cells that would modulate their responses. We tried to distinguish between these possibilities by testing 13 cells in PI and
PL and 23 collicular neurons while the monkey was in total
darkness except for the test stimuli. We selected neurons
that had a clear distinction between real and self-induced
movement. The results of this type of experiment are
shown in Fig. 9 for a cell recorded from PI. The neuron
responded to image motion during fixation and did not
discharge when comparable motion was caused by eye
movements in the light and dark (Robinson and Petersen
1985). All 13 cells in PI and PL gave comparable effects
when tested in the light and dark, and we obtained this
result for 4 cells clearly located in PI and 3 in PL. The same
result was found for all collicular cells tested here, as was
demonstrated previously (Robinson and Wurtz 1976).
To further exclude the possibility of visual interactions in
the saccade condition, we tested 10 cells recorded in PI and
PL while the monkey made saccades to remembered targets
in total darkness (Hikosaka and Wurtz 1983). Figure 10
shows the activity of a neuron with real and self-induced
image movement; there was both a lack of response to the
visual stimulus after the eye movement and a suppression
of activity after the saccade (Fig. 1OB). The suppression was
also present after eye movements made to remembered targets in total darkness (Fig. IOC). These characteristics were
observed in 4 of the 10 neurons tested and indicate that PI
and PL receive an extraretinal signal. Similar properties are
found in cells in the superficial layers of the superior colliculus (Goldberg and Wurtz 1972; Richmond
and Wurtz
C
LIGHT
TOTALDARKNESS
FIG. 10. Activity
with remembered
eye movements in total darkness. A: response of this cell
from PI to a stimulus
swept across its receptive
field during periods of fixation.
As shown in B,
this cell did not respond to the same stimulus
when it was moved across the receptive
field by
saccadic
eye movements.
When the monkey
made eye movements
in total darkness, there was
a suppression
of activity
after the saccade. The
monkey
was rewarded
for making the eye movement to the point where a target light had appeared previously.
TY478a
100 MSEC
REAL
AND
SELF-INDUCED
1980; Robinson and Wurtz 1976). For the six remaining
cells tested in this way, five discharged to the stimulus motion generated by eye movements and had no suppression
with remembered eye movements in total darkness; the
other neuron did not respond to self-induced motion and
had no suppression in the dark. An additional 25 cells not
investigated with real and self-induced
movement were
studied with eye movements in the dark; of all 35 cells
tested, 16 had suppression with eye movements.
For 13 neurons in this sample, we also flashed stimuli in
the receptive field at varying times before and after eye
movements to determine excitability changes (Robinson et
al. 1990). Those cells that had a suppression of activity with
A
E+
15. LOG
OBJECT
MOTION
493
remembered eye movements in total darkness also had a
reduction in excitability (4/ 13, 3 1%) and conversely, those
without suppression in the dark had no change in their excitability (6/ 13,46%). Three neurons with increased excitability after eye movements had either no suppression with
remembered eye movements (n = 2) or a slight increase in
activity (n = 1).
Intensity
ofmodulation
In PI and PL, a number of the neurons completely failed
to respond to stimuli that crossed their receptive fields during eye movements
(Figs. 4A, 9, and IOB), To test the
strength of the processes that prevent responses during eye
movements, we increased the intensity of the stimuli for 23
cells in PI and PL and 12 cells in the superior colliculus that
had no response to our standard stimuli. For 14 cells in PI
and PL and 9 collicular neurons, responses with eye movements began to appear with stimuli 2.1 log units above
background (Fig. 11). For the balance of the cells tested in
this way, responses began to appear with stimuli 3.1 log
units above the background.
We conclude from these experiments that the suppressive process is not absolute.
DISCUSSION
We compared responses of cells to real stimulus movement during periods of fixation with motion that was produced by eye movements.
We have demonstrated
that
many cells in PI and PL respond weakly, if at all, when
motion is caused by eye movements. Similar properties are
common in the superficial layers of the superior colliculus.
When the same experiment
is conducted in the dark,
thereby eliminating visual stimulation of the surround of
the visual receptive field, the result is similar. Also, some of
these same cells have a reduction in activity after eye movements made in total darkness. Thus these cells receive an
extraretinal signal. This input probably prevents cells in PI
and PL from responding to visual stimulation produced by
eye movements.
In discussing our data we will first consider the functional
contributions
these neurons might make. Then we will relate our data to other experiments that have addressed the
issue of vision during eye movements.
1.5 LOG
21. LOG
Functional
31. LOG
RY216 H
FIG. 11.
Effects of increasing stimulus intensity. -4: a cell recorded from
PL. B: a superior collicular
neuron.
Top pair: responses of cells to standard
stimuli swept through
the receptive
field during fixations.
Second pair:
response to self-induced
motion
when the intensity
of the stimulus
was
equal to that of the moving
stimulus
(1.5 log units above background).
Bottom two pairs: responses to self-induced
movement
when the intensity
was increased to 2.1 and 3.1 log units, respectively.
implications
There are cells within PI and PL that incorporate visual
and eye movement signals. Such neurons may be organized
to encode stimulus salience, participate in the initiation of
motor responses, function in motion perception, or reflect
the reduction in vision during eye movements (Chalupa
1990). It is possible that signals from these cells are part of a
system for selecting interesting objects from visual space,
for encoding the salience of the visual stimuli. These neurons are visual in nature, although they are not very selective (Bender 1982; Petersen et al. 1985). As we have demonstrated here, they do receive suppressive signals that eliminate self-induced
stimulation.
We have also reported a
facilitation of these neurons before eye movements (Petersen et al. 1985). Taken together these properties would be
helpful for those systems using salience, those operating to
choose the next image to be processed by fovea1 vision.
494
ROBINSON
The visual processing we have studied may be part of a
system leading to the initiation of movement. Those parts
of the brain that start eye movements to salient images and
those that initiate somatic movements to such targets need
signals that are uncontaminated
by self-generated motion.
Because cells in PI and PL respond -64 ms after visual
stimulation (Petersen et al. 1985), there is adequate time for
their signals to be transmitted
to other brain structures.
Previous studies in the cat have shown that stimulation of
the pulvinar can affect oculomotor
neurons (Wilson and
Goldberg 1980). However, because eye movements can be
started after lesions of the pulvinar, this part of the brain
cannot be the sole site of initiation (Bender 1988; Ungerleider and Christensen
1977, 1979).
When one class of cells in PI and PL discharges (Fig. 4A),
this indicates the presence of images in the external environment. Because the cell responses are suppressed with eye
movements, they are not contaminated with self-induced
stimulation.
At the simplest level, these cells might help
produce the conscious perception of motion. However,
there are several limits to this interpretation.
PI and PL
neurons are not well tuned for the direction of motion nor
for orientation (Bender 1982; Petersen et al. 1985). We
have demonstrated
here that these cells are not well tuned
for stimulus speed (Fig. 3). Given the modest visual properties of these cells, it is unlikely that these individual neurons
encode motion perception. However, a population signal
might encode more precise data (McIlwain
1975, 1976).
Furthermore,
if signals from the present cells were combined with those in the middle temporal area that are well
tuned for motion (Baker et al. 198 1; Maunsell and Van
Essen 1983), then a more appropriate construct might be
present.
Cells in PI and PL could reflect the suppression of vision
during saccadic eye movements. Although there are qualitative similarities between the physiology and perception,
there are clear differences. Saccadic suppression
appears
much less intense (0.5 log units) than the effect we report
here (Riggs et al. 1982). Another difficulty is that some studies have suggested that purely visual factors can account for
the perceptual effect, whereas our cells receive an extraretinal signal. MacKay (1970) showed that rapid movement of
the visual scene produces an elevation of threshold comparable with that found in saccadic suppression experiments.
Others have shown that visual stimulation just before or
after an eye movement will eliminate any vision during the
saccade. This is true for perception as well as for activity of
cells in striate cortex (Campbell and Wurtz 1978; Judge et
al. 1980).
Other studies ofvision during eye movements in primates
Previously we demonstrated
that cells in the superficial
layers of the superior colliculus, like those in PI and PL,
respond over a wide range of stimulus speeds, do not discharge to visual stimuli during saccadic eye movements,
and can be induced to respond to bright images during eye
movements (Robinson and Wurtz 1976). In the superior
colliculus there is an inhibition with eye movements in the
dark, and there too this input is most likely the source of
response reduction with saccades. The superficial layers of
ET AL.
the superior colliculus project to PI and PL (Benevento and
Fallon 1975; Harting et al. 1980; Marrocco et al. 198 1;
Partlow et al. 1977; Raczkowski
and Diamond 1978). We
propose that these collicular properties are conferred onto
the neurons we have studied in PI and PL. This pathway
might seem functionally
quiescent, because collicular lesions have no effect on the visual responses of neurons in
PI, whereas striate lesions completely silence the area
(Bender 1983). However,
striate cortex may provide the
visual inputs to PI cells whereas the colliculus provides the
nonvisual mechanisms
that suppress responses with eye
movements.
Many studies of the primate visual system have shown
eye movement-related
effects on visual responses. In the
squirrel monkey, there is a decrease in excitability in the
magnocellular layers of the lateral geniculate nucleus with
eye movements in the dark (Bartlett et al. 1976). Depression followed by facilitation was also observed in the visual
cortex (Bartlett et al. 1976). There were minimal changes in
geniculate activity related to eye movements in the dark
(Biittner and Fuchs 1973), although stimulation of the reticular formation
significantly
influenced
transmission
through the lateral geniculate (Cohen et al. 1969). Cells in
striate cortex can respond equivalently to motion whether
it is caused by real image movement or by saccadic eye
movements (Fischer et al. 198 1; Wurtz 1969). However,
others have described cells in striate cortex that respond
differently to real and self-induced motion (Battaglini et al.
1986). PI and PL project to the most superficial layers of the
striate cortex (Benevento and Rezak 1976; Ogren and Hendrickson 1976, 1977); if striate cells in layer I receive eye
movement modulations they may not have been sampled
because of the difficulty of isolating these neurons.
Initial studies of area 17 reported equivalent responses
for real and pursuit-generated
motion (Fischer et al. 198 1).
Recent experiments have reported that a small fraction of
cells respond differently to self-induced movement when it
is generated by tracking (Galletti et al. 1984). A subset of
cells in V2 and area 19 responded differently to real and
self-induced movement. This was true for both saccadic
and smooth pursuit movements (Battaglini et al. 1986;
Fischer et al. 198 1; Galletti et al. 1986, 1988).
Overview
Our work and that of others has shown that cells in PI
and PL are visual in nature, although they are not very
selective for stimulus features (Bender 1982; Petersen et al.
1985). The present and previous studies show that these
same neurons are modulated by various eye movement
conditions (Acuna et al. 1983; Perryman et al. 1980; Petersen et al. 1985; Robinson and Petersen 1985; Robinson et
al. 1990). Their visual responsescan be suppressedafter eye
movements, making them lessaccessibleto visual stimulation, and their activity can be adjusted by eye position.
Many of these properties are present in the cells of the superficial layers of the superior colliculus, which are afferents to both PI and PL (Benevento and Fallon 1975; Benevento and Standage 1983; Marrocco et al. 198 1; Partlow et
al. 1977; Raczkowski and Diamond 1978). We hypothesize
that the modulatory influences in PI and PL come from the
REAL
AND
SELF-INDUCED
superficial layers of the superior colliculus, although the
visual properties come from the cortex (Bender 1983). The
dominant efferents from PI and PL go to striate and prestriate cortical areas (Benevento and Rezak 1976; Kennedy
and Bullier 1985; Lin and Kaas 1979). We propose that the
modulated visual signals in PI and PL are projected to these
visual cortical areas and might be used for establishing visual salience. Such signals might be used eventually for attentional purposes or for triggering motor responses.
We appreciate
the technical
help of G. Creswell, L. Cooper, C. Crist, T.
Ruffner,
A. Ziminsky,
and C. Scoutaris; we are also grateful for the help of
J. Steinberg and B. Zoltick
in preparing
this manuscript.
Present address of S. E. Petersen: Dept. of Neurology
and Neurological
Surgery, Washington
University
School of Medicine,
St. Louis, MO 63 110.
Address for reprint requests: D. L. Robinson,
Section on Visual Behavior, Laboratory
of Sensorimotor
Research,
National
Eye Institute,
Bldg.
10, Rm. lOClO1,
Bethesda, MD 20892.
Received
19 November
1990; accepted
in final form
16 April
199 1.
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