Download Ventral Intraparietal Area of the Macaque: Anatomic Location and

.I~URNALOF
Vol. 69. No.
Ventral Intraparietal Area of the Macaque: Anatomic
Visual Response Properties
Location and
CAROL L. COLBY, JEAN-RENE
DUHAMEL,
AND MICHAEL
E. GOLDBERG
Laboratory e ofSensorimotor
Research,
National
Eve
Institute,
Bethesda,
Mawland
20892
.
s
4
SUMMARY
AND
CONCLUSIONS
I. The middle temporal area (MT) projects to the intraparietal
sulcus in the macaque monkey. We describe here a discrete area in
the depths of the intraparietal
sulcus containing neurons with response properties similar to those reported for area MT. We call
this area the physiologically
defined ventral intraparietal
area, or
VIP. In the present study we recorded from single neurons in VIP
of alert monkeys and studied their visual and oculomotor
response properties.
2. Area VIP has a high degree of selectivity for the direction of a
moving stimulus. In our sample 72 / 88 ( 80% ) neurons responded
at least twice as well to a stimulus moving in the preferred direction compared with a stimulus moving in the null direction. The
average response to stimuli moving in the preferred direction was
9.5 times as strong as the response to stimuli moving in the opposite direction, as compared with 10.9 times as strong for neurons
in area MT.
3. Many neurons were also selective for speed of stimulus motion. Quantitative data from 25 neurons indicated that the distribution of preferred speeds ranged from 10 to 320” /s. The degree
of speed tuning was on average twice as broad as that reported for
area MT.
4. Some neurons (22 /4 1 ) were selective for the distance at
which a stimulus was presented, preferring a stimulus of equivalent visual angle and luminance presented near (within 20 cm) or
very near (within 5 cm) the face. These neurons maintained their
preference for near stimuli when tested monocularly,
suggesting
that visual cues other than disparity can support this response.
These neurons typically could not be driven by small spots presented on the tangent screen (at 57 cm).
5. Some VIP neurons responded best to a stimulus moving
toward the animal. The absolute direction of visual motion was
not as important for these cells as the trajectory of the stimulus:
the best stimulus was one moving toward a particular point on the
face from any direction.
6. VIP neurons were not active in relation to saccadic eye movements. Some neurons ( 1O/ 17) were active during smooth pursuit
of a small target.
7. The predominance
of direction and speed selectivity in area
VIP suggests that it, like other visual areas in the dorsal stream,
may be involved in the analysis of visual motion.
INTRODUCTION
The parietal cortex of the macaque monkey receives visual input from the middle temporal area (MT) in the superior temporal sulcus. Maunsell and Van Essen ( 1983a) first
showed that this projection terminates in the depths of the
intraparietal sulcus, in an area that they named the ventral
intraparietal area, or VIP. The existence of this projection
suggested that the intraparietal sulcus should contain an
902
area with visual properties similar to those in area MT. We
report here the existence of such an area and describe its
motion-selective response properties. We refer to this area
as the physiologically defined VIP.
In the present study we examined visual and oculomotor
properties of neurons in VIP with stimuli and testing procedures designed to allow direct comparison with results obtained from previous recordings in area MT (Albright
1984; Maunsell and Van Essen 1983a). We found a motion-selective area confined to the floor of the intraparietal
sulcus and the adjacent deepest portions of the medial and
lateral banks of the sulcus. This physiologically defined area
corresponds to a portion of the MT projection zone. Neurons in this area have direction and speed tuning similar to
that found in area MT, and some VIP neurons are selective
for the distance at which the stimulus is presented. In addition, we found an unusual form of direction selectivity:
some neurons are selective for the anticipated point of contact of a stimulus moving toward the animal, regardless of
the absolute direction of visual motion. In the course of this
study, we discovered that the majority of neurons in VIP
have somatosensory as well as visual responses. The somatosensory properties of VIP neurons will be described in a
separate paper. Preliminary reports of some of these findings have appeared (Colby and Duhamel 199 1; Colby et al.
1989; Duhamel et al. 1989, 199 1).
METHODS
Animal preparation
Three rhesus monkeys ( A4ctc~~cr mhttu) were surgically prepared for chronic neurophysiological
recording by implantation
of ocular search coils, head-holding
devices, and recording
chambers. Surgery was carried out under aseptic conditions by the
use of previously described techniques (Goldberg
1983). Briefly,
monkeys were pretreated with atropine and sedated with diazepam (Valium)
and ketamine hydrochloride.
General anesthesia
was induced and maintained by isofluorane inhalation. Recording
chambers were centered at AP -5.3 and ML 12.2 and placed flat
against the skull. This approach produced electrode penetrations
parallel to the banks of the intraparietal
sulcus rather than in a
standard stereotactic plane. All experimental
protocols were approved by the National Eye Institute Animal Care and Use Committee and certified to be in compliance with the guidelines set
forth in the Public Health Service Guide for the Care and Use of
Laboratory Animals.
Recordings were made with flexible tungsten electrodes introduced through stainless steel guide tubes placed nearly but not
MOTION
SELECTIVITY
quite through the dura. Guide tubes were stabilized by a nylon grid
held rigidly in the recording cylinder (Crist et al. 1988). The grid
served as a guide to produce parallel penetrations down the banks
ofthe intraparietal sulcus. The rigidity of the system and the atraumatic nature of the electrodes allowed us to perform a large number of penetrations
in each hemisphere. Electrode penetrations
were made parallel to the cortical surface of the sulcus and extended lO- 15 mm deep. Neuronal response properties were assessed at least every millimeter,
beginning at the cortical surface
and continuing until the electrode entered the white matter. Adjacent penetrations were made at a l-mm spacing. A systematic
mapping of response properties in intraparietal
cortex was carried
out over the extent of the sulcus accessible from the recording
cylinder ( 1.8 cm ID). Electrode penetrations performed several
months apart at the same grid locations yielded neurons with similar response types at similar depths. The present report concerns
only those neurons identified physiologically
as being within
area VIP.
Visual stimuli were presented on a large, dimly lit, rear-projection tangent screen placed 57 cm from the monkey’s eye. The
visual stimuli were typically spots of light, 2” diam, generated by a
light-emitting
diode ( LED: 0.2 cd/m*)
mounted on an optic
bench. Stimulus position was set by servo-controlled
mirror galvanometers (General Scanner) under computer control. A second
optic bench contained a projection lamp and an adjustable slit
maker for generating oriented stimuli that were also presented via
mirror galvanometers. A third stimulus, the small fixation point
(0.25’ ) at the center of the screen, was generated by a stationary
LED projector. A fixation point could be placed anywhere on the
screen by using one of the optic bench stimuli. The same small
spots used for testing direction and speed selectivity were also used
for testing saccade and pursuit-related
activity. Whole-field random dot stimuli were presented bvd the use of a hand-held projector.
Other stimuli were used in additional tests as needed to characterize VIP neurons as completely as possible. For testing distance
selectivity, a small (20 x 20 cm) screen could be interposed between the monkey and the tangent screen in such a way that the
monkey’s view of the central fixation point was not obscured. The
distance of the screen from the monkey’s face was adjustable. An
independent projection lamp system, also under computer control, was used to present stimuli on this smaller screen. Hand-held
stimuli were also used: an ophthalmoscope
was used to generate
moving spots and slits displayed on the small screen; small objects
(cotton swabs) were used to assess selectivity for motion toward
and away from the animal. Quantitative data were obtained with
the use of these hand-held stimuli by requiring the monkey to
fixate the central point on the tangent screen while the experimenter presented the stimulus and signaled stimulus onset to the
computer by a switch closure. This method permitted measurement of response amplitude but not response latency.
Stimulus presentation, behavioral monitoring,
eye position and
unit sampling, and on-line data analysis were controlled
by a
PDP- 1 l/73 computer (Goldberg
1983). Cells were studied in a
series of standard tasks.
FIXATION
TASK.
The monkey gazed at a fixation point and
made no eye movement or other discernible response to a second
stimulus flashed or moved elsewhere on the tangent screen. In one
version of the task, the monkey initiated the trial by grasping a bar.
This caused the fixation point to appear, and the monkey had to
foveate it to detect a slight dimming that was the signal to release
IN
AREA
VIP
903
the bar. In the other version of the task, the fixation point appeared, and the monkey was rewarded for holding the correct eye
position for a certain interval. In both versions the monkey was
required to keep his eye within an electronically defined window
(2”) centered on the fixation point. The fixation task was used to
find the receptive field ofthe cell and to study the visual responsiveness of neurons in a situation where the stimulus had no behavioral significance (Wurtz 1969 ).
DELAYED
SACCADE
TASK.
During the fixation period, the stimulus appeared for 5200 ms, and the monkey had to continue to
look at the fixation point for at least 500 and up to 1,500 ms after
the stimulus had disappeared. The monkey’s task was to make a
saccade, after fixation point offset, to the location where the target
had been. The target reappeared 200 ms after a correct saccade,
and the monkey was rewarded for holding this new eye position.
This task was used to dissociate activity related to the appearance
of the stimulus from activity associated with the eye movement
(Hikosaka and Wurtz 1983).
RAMP
AND STEP-RAMP
TASKS.
These tasks were used to measure
neural activity during smooth pursuit eye movements. The monkey began by fixating a central point. After a variable period the
fixation point began to move, and the monkev had to track it for
800-l ,200 ms (ramp task). In the step-ramp task, the stimulus
first jumped to a new position and then began to move (Rashbass
1961).
After a neuron had been isolated, the fixation task was used to
assess receptive-field
properties. The period of fixation per trial
varied pseudorandomly
from 2,000 to 3,000 ms with a 500-ms
intertrial interval. The monkey usually kept his eyes within the
electronically defined fixation window even during the inter-trial
interval. The receptive field of the neuron was located, and its
speed preference was estimated with the use of an ophthalmoscope. The neuron was then tested quantitatively
for direction
selectivity with computer-generated
stimuli. The stimulus was
swept through the receptive held in eight standard directions at the
approximate best speed. Speed selectivity was then tested quantitatively with the use of a stimulus moving at different speeds in the
preferred direction. In these tests for speed and direction selectivity, stimuli were presented in pseudorandom
order until data had
been collected for 16 trials for each stimulus parameter. Other
response properties, such as orientation
and distance selectivity,
were then assessed by hand and documented quantitatively
if appropriate. Finally, eye movement paradigms were run to assess
saccadic and pursuit-related
activity. Data analysis was begun by
measuring the average spike rate in a narrow time window (200
ms for direction, 100 ms for speed ) centered on the peak response.
Baseline activity was measured for 200 ms during the fixation
period preceding stimulus appearance.
After recording was completed,
monkeys were anesthetized
with an overdose of pentobarbital
sodium and perfused through
the heart with 10% Formalin. The brain was blocked and equilibrated with 30”/ sucrose. Frozen sections were cut in the plane of
the grid used for recording so that complete tracks were visible in
single sections. Serial sections, cut at 50 pm and thionine stained,
were used to reconstruct the location of each penetration and the
depth at which direction-selective
neurons were first encountered.
A one in five series was reserved for mvelin staining and was used
to locate myelin borders in relation to the physiologically
determined borders of VIP.
Reconstructions
of the location and extent of VIP were based
on microlesions ( 10 PA for 10 s) made at the end of each experi-
904
C. L. COLBY, J.-R. DUHAMEL,
ment. In the first monkey, after having mapped the intraparietal
sulcus in both hemispheres, we recorded again at each site and
placed a pattern of lesions designed to identify each electrode track
and the depths at which specific types of activity were found. In
the second monkey, marking lesions were placed at the borders of
VIP in one hemisphere. In the other hemisphere an electrolytic
lesion was made to destroy all of VIP. Results from this experiment will be reported in a later paper. The third monkey is still
being used for recording. Estimates of the size of VIP in this animal were made from the grid recording map.
RESULTS
Location
and borders of area VIP
DEFINITION OF VIP. Quantitative
data were
obtained from 107 single neurons in the ventral intraparietal area of 5 hemispheres in 3 rhesus monkeys. Units were
identified as being within VIP on the basis of their response
properties and location within the sulcus. The central portion of the medial bank contains neurons with somatosensory responsiveness and no visual activity. The medial
border of VIP was identified as the point at which we could
first find cells with direction-selective visual responses. The
lateral bank of the sulcus contains the lateral intraparietal
area (LIP). Neurons in LIP have visual and eye movement-related activity ( Andersen et al. 1990b; Barash et al.
199 1a,b; Colby and Duhamel 199 1; Goldberg et al. 1990).
The lateral border of VIP was identified as the point where
we first encountered cells with a strong preference for stimuli moving in a specific direction. At the anterior border of
VIP, visually responsive neurons gave way to purely somatosensory cells in the fundus. At the posterior border,
PHYSIOLOGICAL
AND M. E. GOLDBERG
motion- and direction-selective neurons gave way to visual
cells that were not selective for motion.
LOCATION AND sm 0F AREA VIP IN FIVE HEMISPHERES.
Area
VIP is located in the fundus of the intraparietal sulcus (Fig.
I ). In four hemispheres the extent of the zone physiologically identified as VIP was reconstructed histologically.
Area VIP occupies the fundus along the middle third of the
sulcus. It begins anterior to the end of the annectent gyrus
and extends up from the fundus onto both the lateral and
medial banks of the sulcus. At its maximum
extent, VIP
averages 5 mm mediolaterally
and 8 mm rostrocaudally.
Area VIP is comparable in size with area MT (Gattass and
Gross 198 1; Ungerleider and Desimone 1986a; Van Essen
et al. 1981).
CORRESPONDENCE TO MYELIN-DEFINED REGIONS. Both the
lateral and the medial banks of the intraparietal sulcus contain heavily myelinated zones (Blatt et al. 1990; Colby et al.
1988; Seltzer and Pandya 1980; Ungerleider and Desimone
1986). The physiologically defined area VIP described here
is confined to the more lightly myelinated zone in the fundus of the sulcus. Histological reconstructions from myelinstained sections show that, in the lateral bank, the ventral
border of the densely myelinated zone corresponds to the
physiological border between LIP and VIP (Fig. 2). The
medial bank of the sulcus also contains a heavily myelinated zone that does not overlap the physiologically
defined VIP.
Visual response properties
Quantitative data on direction selectivity were
DIRECTION.
obtained for 88 cells. Most VIP neurons are strongly selecA
M
5mm
FIG. 1. Location of ventral intraparietal area (VIP). The small dorsal view of the hemisphere shows the extent of the
recording zone in the opened up intraparietal sulcus, corresponding to sections A through M. Area VIP is the shaded area in
the fundus. The 5 sections, spaced 1 mm apart, span VIP from caudal (section I) to rostra] (section M) and show reconstructions, made from serial sections, of electrode tracks that entered VIP. The cross-hatched region in each section shows the
extent of cortex containing neurons with the properties defined for VIP. Sections I and J contained a densely myelinated
zone (arrows) in the lateral bank of the sulcus adjacent to but not overlapping area VIP.
MOTION
SELECTIVITY
IN AREA VIP
F’IG. 2. Correspondence between myeloarchitectonic
and physiological borders of ventral intraparietal area (VIP). On
the left. the extent ofthe heavily myelinated zone in the lateral bank is indicated by arrows. A microlesion (a) was made at the
most dorsal recording site in VIP. The’lesion is more clearly seen in the adjacent thionine-stained section (right). The
physiologically defined dorsal border of VIP corresponds to the ventral border of the heavily myelinated zone.
tive for direction of stimulus motion. A typical cell is shown
in Fig. 3. The histograms show the response to a small spot
of light moved through the receptive field in eight different
directions. The polar plot shows the average response of the
cell over 16 trials for each direction. This cell preferred
movement downward and to the right and was very slightly
inhibited by movement in the opposite direction. Motion
perpendicular to the preferred direction evoked a weaker
response.
We used two measures to quantify the direction selectivDI = 1.07
EW=l95~
270°
FIG. 3. Direction selectivity of a single neuron in ventral intraparietal
area with direction index (DI) and bandwidth
(BW). Raster,displays represent trial-by-trial responses to a small spot moving in 8 different directions. The associated
histograms show the summed activity over 16 stimulus presentations. Rasters and histograms are aligned on stimulus onset
(long vertical line). Vertical calibration mark at the left edge of each histogram indicates a firing rate of 100 spikes/s. Tick
marks along the bottom of each histogram are 200 ms apart. Receptive-field location is shown at right. The average response
for each direction is shown on the polar plot in the center. Radial axis represents response measured as spikes per second;
polar axis represents direction of stimulus motion; small circle at center represents level of spontaneous activity.
906
C. L. COLBY.
20-
J.-R.
DUHAMEL.
N = 82
x = 0.86
SD = 0.46
ul
= 158
8
cf ‘O%
22
2
0
0.5
1 .o
DIRECTIONALITY
1.5
>1.5
INDEX
FIG. 4.
Distribution
of directionality
index for 82 ventral
area neurons. This index is based on the difTerence between
stimuli moving in the preferred
and null directions.
intraparietal
responses to
ity of VIP neurons and compare it with that reported for
MT neurons. The first was a standard,direction
index (DI)
based on the response (average spikes/s - baseline) to a
stimulus moving in the preferred direction compared with
one moving in the opposite direction (Baker et al. 198 1).
This index was calculated by the formula
DI T 1 ~ (opposite
response/
preferred
response)
Neurons with a DI near 1 are strongly directional, whereas
those with a value near 0 lack direction selectivity. A value
greater than 1 reflects inhibition (activity drops below the
spontaneous rate) in the nonpreferred
direction, as illustrated in Fig. 3. The distribution of DIs for the population is
shown in Fig. 4. The average DI for 82 cells was 0.86 t 0.46
(SD). Overall, 80% of the neurons tested had a response
that was at least twice as large in the preferred direction as in
the null direction. The average response to the preferred
direction of motion was 9.53 times that to the opposite
direction of motion.
The DI is computed from the responses to only two directions of motion. To quantify the sharpness of direction tuning, we used a second measure that is based on the responses to eight directions of motion. For each cell, we constructed a tuning curve by fitting the data with a linear
Gaussian function of the following form
.\‘l = (1 + /)(, 0.51( ‘, mh,)z/.~l
where ~7~is the firing rate in response to a stimulus
BW=61 O
c89
M.
E. GOLDBERG
in direction -xi. Four parameters (u, h, -v. and s) are free: u
is the minimum firing rate; h is the difference between the
maximum and minimum firing rate; &x0is the preferred direction; and s is the standard deviation of the fitted Gaussian. From this Gaussian we measured the full width at half
maximum to estimate the tightness of tuning for direction.
The mean bandwidth for direction tuning was 129.5” (n =
37). Examples of the variation in direction tuning are illustrated in Fig. 5. For each of three cells, we show a tuning
curve fitted to the data obtained for eight different directions of motion.
Previous investigations of area MT have noted an asymmetry in the number of neurons with particular direction
preferences: for MT neurons recorded in the right hemisphere, there is a significant underrepresentation
of rightward and downward
directions of stimulus motion (Maunsell and Van Essen 1983a). We examined the distribution
of preferred directions for 32 neurons in the left hemisphere
that were tested for 8 directions. There was no significant
asymmetry
in the distribution:
all directions of motion
were about equally represented (x2 test, P > 0.1).
For some cells we tested responsiveness to a large (60 X
60”) random dot stimulus. Out of 23 cells tested, 2 1 responded to the stimulus. For 12 cells, we tested whether the
preferred direction of motion using the random dot stimulus matched the preferred direction for a small spot. All of
the direction-selective
neurons ( 1 1) had matching preferences for the two stimuli; one neuron that responded best to
a stationary, flashed spot also responded best to a stationary, flashed random dot stimulus.
SPEED.
Neurons in VIP are sensitive to speed as well as
direction of stimulus motion. Data from a speed-sensitive
neuron are shown in Fig. 6. Responses were quantified by
measuring average spikes per second during a lOO-ms period centered on the peak response and subtracting the
background rate (measured during fixation before onset of
the stimulus).
The best speed for this neuron was 4O”/s.
Across the population of VIP neurons, there was a range of
preferred speeds and considerable variability in the degree
of selectivity for speed. Representative
tuning curves are
shown in Fig. 7. Responses of four VIP neurons are shown
in which each tuning curve is normalized to its greatest
BW=99’
c373
22 sp/sec
moving
AND
-_____I
34 sp/sec
BW=l 50°
c56
__-_
-____
26 spkec
FIG. 5.
Direction
tuning curves for 3 representative
ventral intraparietal
area neurons.
Polar plots show average responses to 8 different directions
of stimulus
motion.
Central circles indicate average spontaneous
firing rate. Each neuron
shows inhibition
for stimulus
motion in the null direction.
Full width at half-maximum
measures of tuning bandwidth
are
indicated for each neuron.
MOTION
SELECTIVITY
IN AREA
907
VIP
1
20"/sec
5”lsec
I I
200 msec
80" /set
FIG. 6. Responses
Raster and histogram
on abscissa ) .
Degrees/Second
ofa ventral intraparietal
area neuron to a stimulus moving in its preferred
direction
at diflerent speeds.
displays as in Fig. 3. Tuning curve shows peak firing rate as a function
of stimulus speed ( note log scale
response. About one-half of the VIP neurons tested ( 13/
25) were selective for stimulus speed in that the response
decreased on either side of the optimum. The remainder
( 11/25 ) were high pass, responding best to the highest
speed tested. One neuron was untuned, maintaining a response rate above 0.80 of its best response for all speeds.
To compare these results on speed selectivity to previous
findings on area MT, we measured both the distribution of
preferred speeds and the average speed tuning curve for the
5
IO
20
40
SPEED
was)
80
760
population. The distribution of preferred speeds for 25 cells
is shown in Fig. 8. This distribution partially overlaps that
reported for area MT (Maunsell and Van Essen 1983a),
but more neurons in VIP preferred high speeds. To compare the average speed tuning of neurons in MT and VIP,
we used Maunsell and Van Essen’s ( 1983a) procedure and
plotted normalized response curves for each neuron in VIP
and shifted the curves so that the peak responses for all cells
were aligned. Points on either side were then averaged to
produce a population tuning curve (Fig. 9). The average
tuning for speed, measured as full width at half maximum
relative to background, is equivalent to a 64-fold change in
speed. This average tuning is twice as broad as that found in
MT ( Maunsell and Van Essen 1983a).
Selectivity for orientation
is often tested
ORIENTATION.
with a moving bar swept across the receptive field. This
stimulus confounds orientation and axis of motion and is
inappropriate for neurons with strong direction selectivity.
To test for orientation
selectivity alone, a stationary,
flashed bar is the preferred stimulus. VIP neurons generally
respond very poorly to such stimuli. Quantitative data on
orientation selectivity were taken only for the few neurons
320
”
FIG. 7.
Speed tuning curves for 4 representative
ventral intraparietal
area neurons illustrating
the range of tuning for speed. Each curve is normalized
to its highest peak firing rate. Neuronal
responses range from
narrowly
tuned to high pass.
FIG. 8.
intraparietal
10
20
40
80
SPEED (DEGISEC)
Distribution
of preferred
area neurons.
160
320
speeds for the population
of ventral
908
C. L. COLBY,
J.-R.
DUHAMEL,
AND
0.9-
0.7-
0
1
I
l/64
I
l/32
1
l/16
I
l/8
l/4
SPEED
I
I
I
I
I
1
l/2
1
2
4
8
16
RELATIVE TO OPTIMAL
wws)
FIG.
9. Average speed tuning curve for the population
of ventral intraparietal area neurons, including
tuned and high-pass neurons. Speed tuning curves for 25 neurons were normalized
to their highest peak firing rate,
and the peak responses were aligned on 1. Responses on either side of 1
were averaged.
Dashed line indicates average normalized
background
rate
of firing.
(n = 5) that responded adequately to stationary oriented
bars. An example is shown in Fig. 10. This neuron responded to a vertical bar flashed in the receptive field but
responded much less to the same bar presented horizontally. Orientation selectivity was independent of stimulus
length. For each of these orientation-selective
neurons, the
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to the preferred
SELECTIVITY.
Some VIP neurons (22/4 1) are selective for the distance at which a visual stimulus is presented. The neuron illustrated in Fig. 1 1 was tested with
stationary, flashed stimuli presented at three different distances. In each condition the monkey was required to
maintain fixation on a point presented on the tangent
screen at 57 cm. The visual stimulus evoked virtually no
visual response when presented in the receptive field on the
tangent screen. A second, smaller screen was introduced
between the monkey and the tangent screen to allow presentation of the same stimulus, equated for luminance and
visual angle, at a distance of 10 or 5 cm. These near and
ultranear stimuli did evoke a visual response. This neuron’s
preference for ultranear stimuli remained even when one
eye was patched, suggesting that cues other than disparity
were used to determine the location in depth of the stimulus.
Forty-one VIP neurons were tested with lights presented
on the adjustable screen or with hand-held stimuli (small
objects) to determine whether responsiveness could be modulated by bringing the stimulus closer to the animal’s face.
Twenty-two neurons showed systematic changes in responsiveness with distance. Of these, 14 preferred ultranear visual stimuli (presented within 5 cm of the monkey’s face),
6 preferred near stimuli (within 20 cm), and 2 responded
best to far stimuli. These distance-selective neurons usually
could not be driven by any visual stimulus on the tangent
screen. Some exhibited a gradient in level of responsiveness, so that a stimulus became increasingly effective in
driving the cell when presented at nearer distances, whereas
other neurons appeared to have a more sharply delimited
WE
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DISTANCE
0.8-
I
E. GOLDBERG
preferred orientation
axis of motion.
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FIG.
10. Orientation
selectivity
in a ventral intraparietal
area neuron.
Stimulus
was a stationary
bar flashed on for
1,500 ms. Vertical calibration
bar at left of histograms
indicates response rate of 100 spikes/s: tick marks are 200 ms
apart.
I
II
I
III
I
I
I
.&&l,
I
62-314-02
MOTION
SELECTIVITY
5cm
IN AREA
909
VIP
10cm
57 cm
I
I
I
I
I
I
I
I
\
FIG. 1 I.
Distance selectivity in a ventral intraparietal
area neuron. Each panel shows the response to a stimulus presented
at a different distance from the monkey.
Stimuli were equated for size and luminance.
In each condition
the monkey
had to
maintain
fixation on the tangent screen fixation point at 57 cm. Vertical calibration
bar indicates
100 spikes/s: tick marks
are 50 ms apart. Neuron responds best to the closest stimulus.
receptive field. Selectivity for stimulus distance was maintained when cells were tested monocularly.
Distance-selective
neurons were also direction selective.
Many ( 14/22 ) exhibited ordinary, frontoparallel direction
selectivity when tested with stimuli presented on a screen
close to the animal or with hand-held stimuli. Some neurons, however ( 8 /22), also showed a more complex form
of direction selectivity related to stimulus trajectory. These
neurons preferred a stimulus moving toward (6) or away
(2) from the animal. The critical variable for these neurons
was the projected point of contact (or point from which the
stimulus was moved away). The neuron shown in Fig. 12A
responded to a stimulus moved toward the animal on a
trajectory that would (were it continued) contact the chin.
It did not respond nearly as well when the same stimulus
was moved along a path that would contact the brow. Most
VIP neurons have somatosensory
as well as visual receptive
fields and are readily driven by a somatosensory
stimulus
applied when the eyes are covered (Duhamel et al. 1989).
This neuron had a somatosensory
receptive field restricted
to the chin. Although this neuron did exhibit planar direction selectivity to a stimulus presented at 20 cm, its best
response was to a visual stimulus moving toward its somatosensory receptive field. Changes in the monkey’s eye position did not change this neuron’s preference for stimulus
trajectories toward the chin (Fig. 12B). When the monkey
was required to fixate a point on the tangent screen either
23’ above or below the center point, the neuron still dis-
charged only to stimuli approaching the chin and not to
stimuli approaching the brow.
Selectivity for stimulus trajectory was not limited to distance-selective neurons. A few neurons ( y1 = 3) that gave
good direction- and speed-selective responses to stimuli presented on the tangent screen still showed stronger responses
to stimuli approaching the somatosensory
receptive field
from any direction.
The visual response properties described above were assessed by presenting stimuli while the animal maintained
fixation. We used saccade and smooth pursuit paradigms to
examine neuronal activity in relation to eye movements.
SACCADIC
EYE MOVEMENTS.
The primary paradigm used
for testing saccade-related activity was the delayed saccade
task in which a stationary target is flashed in the receptive
field while the animal fixates (Hikosaka
and Wurtz 1983).
The offset of the fixation point instructs the monkey to
saccade to the location where the target appeared. By introducing a delay between target presentation
and performance of the saccade, we can measure separately the cell’s
activity in response to target onset ( or offset) and in relation to the saccade. No VIP neuron discharged immediately before a saccade: of 41 neurons tested with this task,
23 gave exclusively visual responses to stimulus onset, and
18 were unresponsive. The small stationary target is a poor
910
C. L. COLBY, J.-R. DUHAMEL,
AND M. E. GOLDBERG
A
Straight
Toward
Toward
From
Above
-
Forehead
84-012-07
Toward
\
from Above with Eyes Up
ZOOK?
Chin from Above with Eyes Up
Toward
Chin with Eyes Down
20
64-012-08
1A’
FIG. 12. Trajectory selectivity in a ventral intraparietal area neuron. A, tc~pYOU’:stimulus moving toward the brow while
monkey fixates central point on tangent screen. Bottom TOW:stimulus moving toward chin while monkey fixates central
point. Direction of motion (straight toward vs. down and toward) and portion of visual field stimulated (upper vs. lower) are
not as strongly related to response as is projected point of contact of the stimulus. B, tc~p:stimulus moving toward brow while
monkey fixates point 23” above central fixation point. Middle: stimulus moving toward chin while monkey fixates above.
Bottom: stimulus moving toward chin while monkey fixates point 23” below central fixation point.
MOTION
MOVING
STIMULUS
PURSUIT
SELECTIVITY
IN DARKNESS
S
E
62-337-03
13.
.I: response to a stimulus
moving
while the monkey
tixatcs. i? response during
stimulus.
FIG;.
through the reccptivc
field
active pursuit of a moving
stimulus for VIP neurons, and visual responses were weak
compared with those produced by moving stimuli. Two of
the 23 visually responsive neurons gave enhanced visual
responses to a stationary stimulus when it became the target
for a saccade ( Bushnell et al. 198 I). Both of these neurons
were also direction selective.
PIJRSIJI
-1‘. We used ramp and step-ramp parad igms to examme neural activity during smooth pu rsuit. For lo/17
cells tested, neurons were active both during passive stimulation with a moving spot while the animal fixated, and
during active pursuit of the moving spot. For six of these
neurons, the best d irection for pursui t matched the preferred directi on for stimulus motion. For the re maining
four cells, the best pursuit direction was opposite to that
preferred for passive stimulus motion. The neuron shown
in Fig. 13 had a visu al response to a spot m oved through the
receptive field and was driven wh .en the mon key trac ked
that stimulus in total darkness.
A projection from area MT to parietal cortex was first
described in New World monkeys (Spatz and Tigges 1972).
In the macaque, Maunsell and Van Essen ( 1983b) observed a projection from area MT to a portion of the intraparietal sulcus, which they called the ventral intraparietal
area, or VIP. Their observation was confirmed and extended by Ungerleider and Desimone ( 1986), who showed
that MT projects to both the lateral bank and the floor of
the intraparietal sulcus. We describe here a physiologically
distinct area with receptive-field properties strikingly similar to those of neurons in area MT. This area can be distinguished from neighboring regions on the basis of the prominence of direction selectivity. We have reconstructed
the
extent of this physiologically defined area and found that it
is confined to the fundus of the sulcus and so includes only
a part of the region that is connected with MT. Area MT
also projects to cortex in the lateral bank where direction
and speed tu ning are not prominent.
In li ght of the functional hete mrogeneity of the MT-recipient zone in intraparietal sulcus. we propose to restrict the term area VIP to de-
IN AREA
VIP
911
scribe the physiologically distinct zone in the depths of the
sulcus.
Area LIP, in the lateral bank, is adjacent to area VIP.
Although VIP and LIP share visual inputs from areas MT,
MST, FST ( Blatt et al. 1990; Boussaoud et al. 1990; Maunsell and Van Essen 1983b; Ungerleider and Desimone
1986b), and both project to area PO (Colby et al. 1988)
there are many other connections that distinguish between
the two areas. Area LIP has a large number of visual inputs
that have not been observed for area VIP, including inputs
from areas V2, V3, V4, PO, MDP, DP, TEO, and TE (Andersen et al. 1990a; Baizer et al. 199 1; Blatt et al. 1990;
Cavada and Goldman-Rakic
1989; Morel and Bullier
1990). These extensive visual connections point up an important difference between the two areas: although the visual connections of VIP are exclusively with dorsal stream
areas, area LIP is strongly connected with both the dorsal
and ventral streams ( Baizer et al. 199 1; Ungerleider and
Mishkin 1982).
The parietal connections of LIP and VIP also differ. Area
LIP projects to, and receives input from, adjacent area 7a,
both within the sulcus and on the neighboring convexity
cortex (Andersen et al. 1985; Blatt et al. 1990; Seltzer and
Pandya 1986). In contrast, area VIP is connected to lateral
convexity cortex, closer to the tip of the superior temporal
sulcus (STS) and at a distance from the intraparietal sulcus
(Seltzer and Pandya 1986). Unlike LIP, area VIP receives
input from superior parietal cortex as well, including the
adjacent medial bank, caudal area 5 convexity cortex, and
parietal cortex on the medial surface of the hemisphere.
These superior parietal connections provide a route for somatosensory
information
to reach VIP, and Seltzer and
Pandya ( 1986) predicted that the fundus should contain a
region of visual and somatic sensory convergence. These
connectional differences between the fundus and the adjacent lateral bank of intraparietal sulcus suggest that the fundus should be considered a separate area.
Other anatomic findings also suggest that there is a distinct cortical area limited to the fundus. The intraparietal
sulcus has previously been shown to be heterogeneous with
regard to myelo- and cytoarchitecture.
The border between
VIP and LIP can be seen in myelin-stained
sections. The
lateral bank of the intraparietal sulcus contains a heavily
myelinated zone, first identified by Ungerleider and Desimone ( 1986b) or VIP* (VIP-star)
to distinguish it from the
lightly myelinated zone in the fundus, which they called
VIP. In contrast, Andersen and his co-workers
(Andersen
et al. 1990a,b; Blatt et al. 1990) have included the heavily
myelinated zone within area LIP, calling it LIPv. They
found that the cytoarchitectonic
ventral border of LIP
corresponds to the ventral border of the myelin-dense area.
We found that the physiologically
defined border between
LIP and VIP corresponds
to the ventral border of the
heavily myelinated zone.
Further cytoarchitectonic
studies of the intraparietal sulcus have identified a distinct cortical area in the fundus.
Seltzer and Pandya ( 1986) described area IPd, a small area
confined to the depth of the intraparietal sulcus, extending
from a rostra1 border with area 2 to a caudal boundary with
OA cortex, at the beginning of the annectent gyrus. Mediallv it borders on area PE and laterally it abuts area POa.
912
C. L. COLBY,
J.-R.
DUHAMEL,
The borders of IPd thus correspond by location to those of
our physiologically
defined area VIP. In contrast, cytoarchitectonic area POa contains within it the physiologically
and connectionally
distinct area LIP (Blatt et al. 1990).
The cytoarchitectonic
border between IPd and POa may
thus correspond to the physiological border between VIP
and LIP.
In summary, we have dehned area VIP as an area in the
fundus of the intraparietal sulcus with a high concentration
of direction-selective
neurons. The reconstructed physiological borders correspond to previously identified cyto- and
myeloarchitectonic
borders. Further, there are substantial
connectional differences between the fundus and surrounding parietal cortex. Several lines of evidence thus support
the conclusion that there is a distinct area, VIP, confined to
the fundus of the sulcus.
Area VIP is readily identified by its distinctive visual response properties, including selectivity for the direction and
speed of moving visual stimuli. Both the prevalence and the
degree of direction selectivity are comparable to that reported for neurons in macaque MT (Albright 1984; Maunsell and Van Essen 1983a; Tanaka et al. 1986). Specifically,
we found that the mean directionality
index in VIP is 0.86,
as compared with 0.93 in MT, and 80% of VIP neurons
have best direction responses that are twice as strong as
their null direction responses, as compared with 86% of
neurons in MT (Maunsell and Van Essen 1983a). The degree of direction selectivity can also be assessed by comparing the ratio between responses in the preferred and opposite directions. In area VIP, responses in the preferred direction average 9.5 times that in the opposite direction.
Responses in area MT are 10.9 times as strong in the preferred direction ( Maunsell and Van Essen 1983a). Likewise, the mean direction-tuning
bandwidth of 129” in VIP
is roughly comparable with the 105” reported for MT (Albright 1984). One apparent difference between MT and
VIP is in the range of preferred directions represented. In
area MT the distribution
of preferred directions shows an
underrepresentation
of ipsilateral and downward
directions
of motion (Maunsell and Van Essen 1983a). In our sample
there was no significant asymmetry.
Neurons in both VIP and MT are selective for stimulus
speed. Neurons in VIP on average prefer higher speeds and
are more broadly tuned, by a factor of two, than MT neurons. The range of preferred speeds in VIP is a subset of that
found in MT. The shift in the average preferred speed reflects the absence of VIP neurons preferring slow speeds
and the presence of high-pass neurons. Finally, VIP and
MT each contain neurons that are orientation
selective,
even though stationary, flashed bars are poor stimuli for
neurons in both areas.
Previous reports on response properties of neurons in
parietal cortex have not recognized VIP as a distinct area
nor described a sulcal region with these visual properties.
Direction selectivity has been noted in neurons in parietal
convexity cortex at the border between areas 7a and 7b
(Motter et al. 1987; Robinson et al. 1978). Neurons in this
7a/7b border region have very large receptive fields and
AND
M.
E. GOLDBERG
complex types of direction selectivity including radial and
whole-field motion (Motter and Mountcastle 198 1; Steinmetz et al. 1987). Sensitivity to motion in depth and to
disparity change has been observed in neurons in both the
intraparietal and superior temporal sulci (Kusunoki et al.
1991).
Ew. ~novc-‘lnc’nt-r~~lut~~~ at ivit .1’
Neurons in area VIP are active during smooth pursuit
eye movements. The pursuit-related
activity of these neurons could be a purely visual response to target motion or to
the visual input resulting from the eye movement. Extraretinal input, related to the eye movement itself, may also
contribute to these responses, as it does in area MST (Newsome et al. 1988). The only other region of parietal cortex
that contains a concentration
of neurons active in pursuit is
the dorsal bank of the STS, between convexity cortex (area
7a) and MST (Kawano
et al. 1984: Sakata et al. 1983).
Area VIP neurons do not fire in conjunction with saccadic
eye movements. In this regard, area VIP is quite different
from the rest of posterior parietal cortex, where cells active
in relation to saccadic eye movements predominate (Barash et al. 199 1a,b; Gnadt and Andersen 1988; Goldberg et
al. 1990; Mountcastle et al. 1975).
Extrastriate visual cortex in the macaque contains over
two dozen distinct visual areas. These areas are very heterogeneous, differing widely in their size, retinotopic organization, and visual response properties (Colby and Duhamel
199 1: Felleman and Van Essen 199 1; Gattass et al. 1985;
Kaas 1989; Maunsell and Newsome
1987; Van Essen
1985 ). Two basic ideas have been used to describe the organization of these multiple visual areas. The first is that there
is an anatomic hierarchy. Maunsell and Van Essen ( 1983)
established that visual areas could be ordered by placing
any given visual area at a level just above the highest area
from which it receives an ascending projection. Area VIP is
at least one level above area MT and is generally placed at
the same level as areas MST and LIP (Boussaoud
et al.
1990; Colby and Duhamel 199 1; Colby et al. 1988; Felleman and Van Essen 199 1; Maunsell and Van Essen 1983;
Ungerleider and Desimone 1986b). Our physiological results on complex visual response properties in VIP reinforce its placement at a relatively high level in the hierarchy.
A second basic concept in current views of extrastriate
cortex organization is that of processing streams. Ungerleider and Mishkin ( 1982) introduced the idea that extrastriate cortex contains two parallel pathways: a dorsal
stream leading to posterior parietal cortex and a ventral
stream leading to inferior temporal cortex. Area VIP is
clearly a member of the dorsal stream on the basis of its
prominent connections with other dorsal stream areas. Further, the physiological properties of neurons in area VIP
reflect its connectional position in extrastriate cortex: the
speedand direction selectivity of VIP neurons is comparable to that seenin other dorsal stream areas like MT. These
visual responseproperties are common throughout the dorsal stream, including area V3, and are generally lacking in
MOTION
SELECTIVITY
ventral stream areas such as VP and V4 (Burkhalter
et al.
1986; Desimone and Schein 1987; Felleman and Van Essen
1987).
Visudfirnct ions of’
. ma WP
The predominance of neurons selective for direction and
speed in area VIP suggests that this area contributes to the
analysis of visual motion. It is of particular interest that
some VIP neurons appear to be involved in detection of the
trajectory of stimulus motion and anticipation of point of
contact for an approaching visual stimulus. For most of
these neurons, the visual response was tied to the location
of the somatosensory
receptive field, although some purely
visual neurons were also selective for stimulus trajectory.
Previous investigations
have identified similar response
characteristics in periarcuate cortex ( Rizzolatti et al. 198 1 ),
temporal cortex (Mistlin and Perrett 1990) and putamen
(Gross and Graziano
1990) and ocular following
responses have been shown to depend on viewing distance
(Busettini et al. 199 1). Finally,- some VIP neurons were
sensitive to the static distance of visual stimuli and were
usually most sensitive to stimuli presented very close to the
animal. This unusual response could signal the presence of
a target that can be acquired by reach ing with th e mouth.
One special visual function of area V IP may be to detect
and localize stimuli near the face and contribute to eye/
hand and mouth coordination.
More generally, area VIP,
like the other dorsal stream areas it resembles, may participate in the perception of visual motion.
We arc grateful to the stalIof the Laboratory
of Sensorimotor
Research
for their invaluable
support:
C. Crist and T. Ruffner
for machining:
A.
Hays and B. Zoltick for computer
systems support: L. Jensen for electronics; M. Smith for histology:
K. Powell and H. MacGruder
for animal support: Dr. James Raber for veterinary
care: and J. Steinberg and R. Harvey
for facilitating
everything.
Address for reprint requests: C. L. Colby, NIH. Bldg. 10, Rm 1OC 10 1,
Bethesda, MD 20892.
Received
15 June
1992: accepted
in final
form
4 November
1992.
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