Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115-5701
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ABSTRACT |
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Born, Richard T..
Center-Surround Interactions in the Middle Temporal Visual Area
of the Owl Monkey.
J. Neurophysiol. 84: 2658-2669, 2000.
Microelectrode recording and 2-deoxyglucose (2dg)
labeling were used to investigate center-surround interactions in the
middle temporal visual area (MT) of the owl monkey. These techniques revealed columnar groups of neurons whose receptive fields had opposite
types of center-surround interaction with respect to moving visual
stimuli. In one type of column, neurons responded well to objects such
as a single bar or spot but poorly to large textured stimuli such as
random dots. This was often due to the fact that the receptive fields
had antagonistic surrounds: surround motion in the same
direction as that preferred by the center suppressed responses, thus
rendering these neurons unresponsive to wide-field motion. In the
second set of complementary, interdigitated columns, neuronal receptive
fields had reinforcing surrounds and responded optimally to
wide-field motion. This functional organization could not be accounted
for by systematic differences in binocular disparity. Within both
column types, neurons whose receptive fields exhibited center-surround
interactions were found less frequently in the input layers compared
with the other layers. Additional tests were done on single units to
examine the nature of the center-surround interactions. The direction
tuning of the surround was broader than that of the center, and the
preferred direction, with respect to that of the center, tended to be
either in the same or opposite direction and only
rarely in orthogonal directions. Surround motion at various velocities
modulated the overall responsiveness to centrally placed moving
stimuli, but it did not produce shifts in the peaks of the center's
tuning curves for either direction or speed. In layers 3B and 5 of the
local motion processing columns, a number of neurons responded only to
local motion contrast but did so over a region of the visual field that
was much larger than the optimal stimulus size. The central feature of
this receptive field type was the generalization of surround
antagonism over retinotopic spacea property similar to other
"complex" receptive fields described previously. The columnar
organization of different types of center-surround interactions may
reflect the initial segregation of visual motion information into
wide-field and local motion contrast systems that serve complementary
functions in visual motion processing. Such segregation appears to
occur at later stages of the macaque motion processing stream, in the
medial superior temporal area (MST), and has also been
described in invertebrate visual systems where it appears to be
involved in the important function of distinguishing background motion
from object motion.
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INTRODUCTION |
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Center-surround interactions
play an important role in processing sensory information (Allman
et al. 1985b). By allowing a neuron to make a comparison
between activity in a restricted set of "central" inputs
and those in the area immediately adjacent, the interactions can make
explicit even subtle changes in the representation across
the input layer. Since spatial variation is a key feature of objects of
interest to an organism, the center-surround operator is a very
effective means of refining sensory representations and rendering them
more efficient (Attneave 1954
; Grossberg
1983
; Nakayama and Loomis 1974
).
Examples of center-surround receptive field organization
can be found in nearly every sensory domain that has been studied, including vision (Barlow 1953; Hartline
1940
; Kuffler 1953
; Maturana et al.
1960
), audition (Knudsen and Konishi 1978
),
touch (Mountcastle and Powell 1959
), olfaction
(Yokoi et al. 1995
), and electroreception (Bastian 1974
). Center-surround organization is
particularly prominent in the visual system, where it is encountered as
early as retinal bipolar cells (Kaneko 1970
;
Werblin and Dowling 1969
) and at least as late as
extrastriate visual areas such as V4, where it appears to be involved
in comparisons used for processing both form (Desimone and
Schein 1987
) and color (Schein and Desimone
1990
), and the middle temporal visual area (MT) (Allman
et al. 1985a
) and MSTl (Eifuku and Wurtz 1998
),
where it is presumably involved in motion processing.
In motion processing areas, the center-surround organization
of the receptive fields yields interesting properties. Some neurons respond to a short bar of light or a small patch of random dots moving
in their preferred direction, but this response is suppressed as the
stimulus is made larger. In some cases, the response to a small,
centrally located stimulus can be enhanced by opposing motion in the
area surrounding the so-called "classical receptive field" (CRF).
This property has been found in MT neurons in both the owl monkey
(Allman et al. 1985a) and the macaque (Lagae et al. 1989
; Tanaka et al. 1986
) as well as in cat
superior colliculus (Sterling and Wickelgren 1969
) and
lateral suprasylvian area (von Grunau and Frost 1983
),
and in pigeon optic tectum (Frost and Nakayama 1983
;
Frost et al. 1981
). The antagonistic surrounds of these neurons render them insensitive to wide-field motion but sensitive to local motion contrast. Other types of
motion-sensitive neurons have surrounds that reinforce the
center
i.e., the surround's direction preference is similar to that
of the center
the result of which is that they respond best to
wide-field motion (Allman et al. 1985a
; Tanaka et
al. 1986
).
That these two different types of neurons are segregated from each
other within MT of the owl monkey was indicated by 2-deoxyglucose (2dg)
experiments and microelectrode recordings (Born and Tootell 1992). A wide-field random dot stimulus moving coherently at
systematically varied directions, speeds, and binocular disparities
produced patchy regions of high 2dg uptake, termed "bands," and
intervening low-uptake regions, called "interbands." Microelectrode
penetrations showed that the center-surround properties of neurons in
MT were also clustered and that they appeared to correspond to the 2dg patterns. Furthermore, the center-surround properties were similar within a given penetration perpendicular to the cortical surface, suggesting a columnar organization.
In the present study, the relationships between the 2dg band-interband
patterns and single-unit properties are explored in greater
quantitative detail, and further evidence for a columnar organization
is presented. Additionally, the nature of the center-surround relationshipswith respect to tuning for both direction and speed, and
with respect to positional invariance
are examined. These experiments
show evidence for further hierarchical processing of motion cues within
a column.
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METHODS |
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Surgical preparation
All procedures were approved by the Harvard Medical Area
Standing Committee on Animals. One week prior to the experiment, an owl
monkey (Aotus nancymai) was anesthetized with pentobarbital sodium, and, under sterile conditions, a dental acrylic head post was
attached to its skull. On the day of an experiment, anesthesia was
induced with ketamine (15 mg/kg im), the animal was intubated, an
intravenous catheter was inserted, electrocardiographic (EKG) leads
attached, and a blood pressure cuff placed around the arm. Core body
temperature was monitored with a rectal temperature probe and
maintained at 37.5°C by a thermostat-controlled heating pad.
End-tidal pCO2 was continuously monitored and
maintained within physiological limits during electrophysiological
recording. After a loading dose of sufentanil (7.20 µg/kg iv),
anesthesia was maintained with a constant intravenous infusion of
sufentanil (2-8 µg · kg1 · h
1). Adequacy of anesthesia was ensured by
monitoring EKG and blood pressure and supplementing the constant
infusion with an intravenous bolus of sufentanil (1 µg/kg) if either
measure increased 10% or more above baseline in response to a pinch of
the tail or a nail bed. For more rapid control of anesthetic levels, we
often supplemented the sufentanil with a small amount of isoflurane (0.25-0.5% in oxygen). In tests on unparalyzed animals, these measures were sensitive and early indicators of lightened anesthesia, preceding by several minutes any movement by the animal in response to
painful stimuli.
All incision sites were first thoroughly infiltrated with a long-acting
local anesthetic (0.5% bupivicaine with 1:200,000 epinephrine). A
small craniotomy (approximately 2 mm diam) was made with a high-speed
dental drill, after which the underlying dura was bluntly dissected
using fine forceps. After surgical procedures were completed, the
animal was paralyzed with a continuous intravenous infusion of a
combination of gallamine triethiodide (10 mg · kg1 · h
1) and
curare (0.1 mg · kg
1 · h
1).
Optics
After topical infusion of a local anesthetic (proparacaine HCl, 0.5%), corneal curvature was measured with a keratometer, and gas-permeable contact lenses of the appropriate basal curvature were placed over the eyes. The pupils were dilated and accommodation paralyzed with atropine eye drops. The eyes were refracted for the appropriate distance, usually 57 cm, using trial lenses, and a Risley prism was placed over the right eye so that receptive fields from the two eyes could be brought into register.
Stimulus generation and data acquisition
Stimuli were generated by a Silicon Graphics IRIS 3130 computer and displayed on a Sony Trinitron color monitor with resolution of 1,024 × 786 pixels at a 60-Hz noninterlaced refresh rate. Stimuli could be controlled either manually, using a mouse and a "dial-and-button" box, or by a second computer via a serial port interface. This second computer also collected and stored the unit data using a counter-timer board (Metrabyte CTM05).
Neuronal signals were recorded using glass-coated tungsten
microelectrodes (Merrill and Ainsworth 1972) with
standard amplification and filtering. Single units were isolated on the
basis of constant spike height and waveform. When a unit was
encountered that could be clearly discriminated from the background
activity, it was studied using a variety of stimuli including bars,
spots, annuli, gratings, and random dots. It was attempted to resolve
single units approximately every 100 µm to obtain adequate spatial
sampling. In situations where this was not possible, multi-unit
activity was recorded.
Once the location of the receptive field was found, its borders were
mapped with a light bar using the minimal response technique (Barlow et al. 1967). This region will be subsequently
referred to as the CRF. The optimal direction, speed, and binocular
disparity were determined qualitatively by listening to the spike
output on a loudspeaker. In all subsequent tests, these qualitatively optimized parameters were used and held constant from trial to trial.
If the neuron responded as well to stimuli presented to one eye as it
did to any combination of the two eyes (determined by adjusting the
Risley prism while listening to the cell's spike output), it was
tested monocularly. In cases where the neuron responded well only to
binocular stimuli at a particular disparity, the best disparity was
used for subsequent testing. The neuron's optimal stimulus (random
dots vs. a single bar), and the overall response to a large field of
random dots were also recorded.
Quantitative tests
Quantitative data were collected using a personal computer (PC) to coordinate stimulus presentation and record spike arrival times in the form of peristimulus time histograms (PSTHs). Data were analyzed and displayed graphically on-line showing the unit's response before, during, and after stimulus presentation as a function of a given stimulus parameter value. Stimuli were presented in a blockwise random order with a minimum of five repetitions of each stimulus.
Two basic measures of center-surround interactions were used: an area summation test (Fig. 1A) in which the response of the cell was measured as a function of the aperture size of a circular patch of moving random dots (dot density constant) centered in the CRF, and the surround direction test (Fig. 1B), which involved sweeping an optimally oriented bar (constant on all trials) across the center of the CRF while the direction of motion of a large surround annulus of random dots was varied from trial to trial. The area summation curve (ASC) provided information on the size, strength, and polarity of the surround. The surround direction test was an important supplement to the area summation test since many interband neurons did not respond well even to small patches of random dots but did respond well to bars.
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Data analysis
Area summation test data were analyzed in two ways. First, the
slope of the regression line was used a measure of the strength of
surround antagonism (SA). For curves that showed a rising limb before a
falling limb (e.g., Fig. 6A), the regression line was fit to
the falling limb. This was only done when it was clear that suppression
was the dominant effect of the surround and, in nearly all cases,
simply meant excluding the first point (smallest aperture size) from
the regression. Each neuron was also classified as having either
"strong," "weak," or "no" SA. Cells from which area
summation data were obtained were classified according to the slope of
the regression line fit to this data: strong SA, slope less than
0.03; weak SA,
0.03
slope < 0; and no SA, slope
0 or not significantly different from 0. At sites where quantitative
area summation data were not obtained, cells were classified based on a
qualitative comparison of the response to wide-field stimuli, such as
large random dot patches and gratings and small, discrete stimuli, such
as bars and spots. As a second measure of center-surround interaction,
a surround index (SI) was calculated to compare the response to small
field (SF) and wide-field (WF) motion: (WF
SF)/(WF + SF).
Values approaching
1 indicated strong SA; values approaching +1
indicated strong area summation. Surround direction test data were fit
with a Gaussian having four free parameters: amplitude, offset, mean
and standard deviation. The mean and standard deviation parameters were
used as a measure of the direction preference and the tuning bandwidth [full width at half height = 2.36*sigma (Carney and
Shadlen 1993
)], respectively.
Histological reconstructions
During each electrode penetration, from two to five lesions were made by passing current through the electrode tip (1.5-2.5 µA for 1-2 s, electrode negative) to serve as markers for subsequent track reconstructions. The standard practice was to locate a recording site at which to make a lesion, record cells beyond this for 150-250 µm, and then back up to make the lesion. Five to 10 min after backing up to the site, the unit properties were reconfirmed prior to making the lesion. This technique was a compromise designed to prevent large gaps in data collection around the lesion while still permitting precise correspondence between the physical lesions and the microdrive readings.
2dg
For four of the oblique penetrations, at the end of the
physiology recording the band-interband patterns were labeled with 2dg
(Kennedy et al. 1975; Tootell et al.
1988
). The stimulus monitor was moved in to 28.5 cm, and the
animal's eyes were again refracted before inserting a recording
electrode into striate cortex. A perifoveal, binocular single unit was
then isolated to align the eyes using the Risley prism.
Ten minutes prior to infusion of the 2dg, the animal was given an
injection of methamphetamine (50 µg/kg im) while heart rate, blood
pressure, and cortical activity were monitored to ensure that the level
of anesthesia remained adequate. An increased level of catecholamines
has been reported to sharpen cortical columns labeled by 2dg
(Craik et al. 1987). Subsequent experiments in four
animals showed that this dose of methamphetamine did not qualitatively
affect the patterns
compare the 2dg pattern in Fig. 6 (obtained
with methamphetamine) with those in Fig. 7 (obtained without methamphetamine)
although it did tend to improve
the contrast. During infusion of the 2dg, the animal viewed a large
field of random dots that moved in systematically varied directions
(15° increments) and speeds (10, 15, 25°/s) over the 45 min of the experiment. In some experiments, the density of the random dot display
(0.5, 1, and 2%) and the binocular disparity (±2 diopters) were also
varied, but neither manipulation affected the patterns so obtained. The
2dg (50-200 µCi/kg; 2-[1-14C]deoxyglucose; American Radiolabeled
Chemical, St. Louis, MO) was infused slowly over the first 10 min to
avoid bias in uptake caused by any single stimulus condition. After 45 min, the animal was deeply anesthetized with pentobarbital sodium (50 mg/kg iv) followed by intracardial perfusion and fixation (0.9% NaCl,
13% sucrose followed by 2.5% glutaraldehyde/0.7% formaldehyde in 0.1 M PB, pH = 7.4 also with 13% sucrose). The brain was quickly
removed from the cranium, the cortical sulci were unfolded and each
hemisphere was flattened and then immediately frozen on a glass slide
placed on top of a metal block that had been cooled with dry ice
(Tootell and Silverman 1985
).
Sections were cut on a cryostat (Frigocut 8000; 40 µm) parallel to
the cortical surface and placed on subbed coverslips. The coverslips
were glued to 20 × 25 cm sheets of cardboard, then apposed to
X-ray film (Kodak MinR) for periods of 1-6 wk, depending on the amount
of isotope infused. Once satisfactory autoradiographs were obtained,
alternate sections were processed for cytochrome oxidase (CO)
(Wong-Riley 1979) or Nissl substance or both.
For perpendicular microelectrode penetrations, 2dg labeling was not performed because earlier experiments had shown that the craniotomy overlying the electrode track caused intense, artifactual 2dg uptake that obscured any patterns that might have been present. On completion of the unit recording, the animal was perfused, under deep barbiturate anesthesia, with 1 l of 0.9% NaCl followed by 2-3 l of 2.5% glutaraldehyde and 0.7% formaldehyde in 0.1 M PB (pH 7.4). The brain was removed from the skull, and the tissue was blocked in the coronal plane and dropped into a chilled solution of 15% sucrose in 0.1 M PB. This was kept on a shaker tray at 4°C for 1-2 days then transferred to a 30% sucrose solution for another 2-3 days. After this, 60- to 80-µm-thick sections were cut in the coronal plane on a freezing sliding microtome, mounted onto subbed glass slides, and stained with cresyl violet.
Electrode track reconstructions
For perpendicular penetrations, the section containing the
lesions was photographed through a microscope (Zeiss Axioskop) using
brightfield illumination. Laminar boundaries were located on the
photograph and their location relative to the lesions was used to
assign each boundary a number in electrode track coordinates. In this
way, each recording site was assigned to one of seven specific layers:
1 (from which no data were recorded), 2/3A, 3B (distinguished by the
presence of large pyramidal cells), 4 (granular cortex), 5, and 6A
[arbitrarily defined as the first 50 µm of layer 6, which also
receives inputs from V1 (Rockland 1989)] and 6B.
For oblique penetrations, the electrode track reconstructions were somewhat more involved because the tissue was sectioned parallel to the surface of the flattened cortex. The lesions were first located on different CO sections. These sections were scanned into an image processor so that subsequent images could be aligned using the patterns of radially penetrating blood vessels as guides. The horizontal progress of the electrode track was charted from section to section, and each successive section was kept in register within the computer's memory. The reconstructed track was superimposed on the 2dg patterns that had been scanned in at the same magnification, again using blood vessels and tissue artifacts as guides for alignment. Using the distances between lesions and the corresponding microdrive readings for the lesion sites, a scaling factor was computed, which then allowed each recording site, identified by a microdrive reading, to be located on the CO and 2dg images.
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RESULTS |
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Over the course of 21 microelectrode penetrations (10 oblique, 11 perpendicular) in 18 monkeys, data were recorded from 384 different cortical sites. A single unit was isolated at 288 sites (75%); multi-unit activity was recorded at the remaining 96 sites (25%). Due to time constraints or technical problems, such as losing isolation of the neuron, quantitative data were not recorded at every site. A total of 201 area summation tests and 169 surround direction tests were performed.
Center-surround interactions
A variety of center-surround interactions were encountered (Fig.
2), but these could be categorized into
two major groups. This was indicated by strong statistical evidence for
a bimodal distribution of our quantitative measures of center-surround
interaction (Fig. 2, top), such as the slope of the
regression line fit to ASC data (Shapiro-Wilk W test,
W = 0.923, P < 0.0001) and the SI
(W = 0.908, P < 0.0001). One group was
characterized by surrounds that were directionally
antagonistic to the center. Because of this property, none
of these neurons responded well to WF motion regardless of the
direction, speed, or binocular disparity of the stimulus. Within this
group of local motion processing neurons, there was a continuous range
of selectivity of the surround for direction. At one extreme were
neurons that responded most vigorously when a centrally placed bar or
small random dot patch was surrounded by an annulus of random dots
moving in the opposite direction, as first described by
Allman and colleagues (1985a). On the two quantitative
tests, this receptive field type was usually characterized by an ASC
that fell off dramatically as the random dot patch size increased, and,
on the surround direction test, a rather sharply tuned surround that
was able to both "push" and "pull" the response with respect to
the center alone. This latter property is illustrated Fig. 2, top
right. The neuron gave a good response to a single bar swept
across the center of its receptive field (bar plot labeled "B"),
gave no response to an annulus of random dots, showed strong suppression of the bar response when the dots in the annulus moved in
the same direction as the center bar (0°), and showed
strong facilitation when the surround dots moved in the
opposite direction (180°). This type of push-pull behavior
occurred in just under a third of the neurons that had antagonistic
surrounds. For another third (Fig. 2, middle right), the
surround was clearly direction-selective but showed only
antagonistic effects with the suppression being minimal when the
surround moved in the opposite direction to that of the center. The
remaining third of the neurons with antagonistic surrounds showed
suppression of the center response by surround motion in any
direction (Fig. 2, bottom right).
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Another characteristic of the group of cells with antagonistic
surrounds was the tendency for discrete objects, such as bars or spots,
to be much better stimuli than textures, such as gratings or random
dots. This can be seen by comparing the ASC with the surround direction
curve for the neuron in Fig. 3. The
neuron responded poorly to random dot patches of any size, yet a single bar swept across the center of the receptive field (RF) gave a vigorous
response. This was true of the population in general: there was a
strong relationship between the qualitative rating of neurons as dot or
bar cells and the absence or presence of antagonistic surrounds,
respectively (2 test, P < 0.0001).
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The other major group of neurons responded best to WF motion. In many cases, the region of increasing response, as measured by the ASC, greatly exceeded the area mapped using a single bar. This difference may have been a matter of threshold, since a response could usually be elicited by using an annulus of random dots that completely excluded the CRF. Such behavior would indicate that these regions are perhaps more properly thought of as an extension of the center rather than as a surround proper. Nevertheless it was true that excitatory regions beyond the CRF were most frequently observed in neurons outside of the input layers: compare, for example, the ASCs of neurons 12-15 of Fig. 4, recorded from layer 4, with those from neurons 16-20, which were recorded from layer 5. This finding makes it likely that these regions represent the result of further processing within MT, and it remains possible that further study may reveal other differences between them and the CRF. Thus the excitatory regions beyond the CRF will henceforth be referred to as reinforcing surrounds.
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Anatomical organization
In an earlier report (Born and Tootell 1992), we
demonstrated that the qualitatively determined center-surround
properties were clustered along oblique microelectrode penetrations,
appeared to correspond to the 2dg band-interband patterns, and were
similar along perpendicular penetrations. In the following paragraphs, the quantitative aspects of this anatomical organization will be
explored in greater detail.
Figure 4 shows the results of a single, oblique penetration spanning 2 mm of the cortex. Surrounding the penetration are the ASCs for all 22 units recorded at approximately 100-µm intervals. Examining these curves reveals several clusters sharing common shapes, indicative of similar types of center-surround interactions: units 1-4 show a general lack of surround suppression, units 5-10 all show significant surround suppression, units 11-14, all recorded in layer 4, show very little influence of the regions beyond the CRF (whose boundaries are indicated by the vertical, dotted lines), and units 16-22 show evidence for significant facilitation beyond the CRF. While the transitions in this penetration appear quite abrupt, it was not unusual to find "transitional" ASCs that showed only weak surround suppression between regions of strong suppression and facilitation.
The quantitative evidence for clustering of center-surround
interactions across all penetrations was examined by the method previously used to analyze the organization of binocular disparity in
the cat (LeVay and Voigt 1988) and macaque monkey
(DeAngelis and Newsome 1999
). For each pair of recording
sites within a given penetration, the absolute value of the difference
in the SI (|
SI|) is plotted as a function of the distance
between the recording sites (Fig. 5). In
most cases, the single units were not sampled at precisely regular
intervals so the distances were first grouped either to the nearest 200 µm (Fig. 5A) or, for examining longer-range interactions,
to the nearest 300 µm (Fig. 5B). If there exists an
overall organization for the measured index, then recordings from
nearby locations should show smaller differences than recordings from
distant locations.
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This relationship is precisely what was found. For oblique penetrations
(), the difference values approach and then exceed the difference
value that would be expected by chance (the average |
SI|
obtained by randomly selecting 10,000 pairs of recording sites from the
entire data set). The strong similarity between recording sites
separated by distances of 2.1-2.4 mm (Fig. 5B) is
consistent with the band-like periodicity suggested by the 2dg patterns
(Figs. 6 and
7). The difference values for
perpendicular penetrations (
) were always smaller than the
corresponding oblique values, consistent with an overall columnar
organization. A similar picture was obtained for both oblique and
perpendicular penetrations when the slope of the ASC was used as the
measure of center-surround interactions.
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To further examine the effects of penetration angle and distance
between recording sites, a two-way ANOVA was performed. For both
dependent measures (|SI| and |
ASC slope|) and for both site distance groupings (200 or 300 µm), the two main effects were
highly significant (P < 0.01). However, in no case was
the interaction term between site distance and penetration angle
statistically significant (P > 0.5), consistent with
the observed similarity in slopes between the plots for oblique and
perpendicular penetrations.
This analysis of the perpendicular penetrations revealed a somewhat
greater intracolumnar variability than expected. Although the
difference values between recording sites within a column were always
less than would be predicted by chance and always smaller than those
for oblique penetrations, they nevertheless rose quite steeply with
site distance over the first 0.5 mm (Fig. 5A, ). This may
reflect a relatively weak columnar organization but might also be
explained by variability in the angle of the penetration. To see if the
latter was the case, the analysis was re-run using only those
perpendicular penetrations (6 of 11) in which the electrode track made
an angle of less than 10° with respect to the radial fibers. When
this was done (Fig. 5A,
), the slope of the line became
much flatter, and this was reflected by a significant interaction term
in the two-way ANOVA (P < 0.05).
Thus overall this analysis provides a picture of a local columnar organization with a tendency toward periodicity at a wavelength of approximately 2 mm. This repeat distance is somewhat longer than the periodicity observed in the 2dg patterns but can be explained by two factors. First, the oblique penetrations were not perfectly parallel to the cortical surface and second, the consistent direction of the electrode penetrations, from posterior to anterior, was not strictly perpendicular to the long axis of the 2dg bands, which tend to arc around and run nearly parallel with the STS (see Figs. 6 and 7).
That the 2dg band-interband patterns reflect the clustering of neurons with similar center-surround properties was confirmed by a direct correlation of the two measures (Fig. 6). This was done for four oblique penetrations in four different animals after which a 2dg experiment was performed. For each penetration, the electrode track was superimposed on the 2dg autoradiograph, and the gray-level value underlying each recording site was determined. To permit comparisons between animals, each gray level value was normalized to the range of values found within MT for that animal. The results of this analysis show that for both the SI and ASC slope, the correlation was highly significant (SI: r2 = 0.565, P < 0.0001; ASC slope: r2 = 0.534, P < 0.0001) and in the expected direction: neurons whose RFs had strongly antagonistic surrounds were located in the lightest regions of the 2dg autoradiographs (light indicating low 2dg uptake to the WF motion stimulus) and vice versa.
Finally, additional evidence that the overall organization is columnar
comes from the laminar consistency of the 2dg patterns themselves (Fig.
7). A comparison of the four panels in this figure shows the same basic
features extending from the most superficial to the deepest layers. As
is typical for 2dg patterns, they tend to be sharper and of higher
contrast in the middle layers and more diffuse in the deep layers
(Geesaman et al. 1997; Tootell and Hamilton
1989
; Tootell et al. 1988
). Typically the
highest contrast patterns were seen in the lower part of layer 3 (Fig. 7B). No apparent narrowing of the 2dg columns was observed
in layer 4, even though this layer, along with the very thin uppermost part of layer 6 (both of which receive inputs from V1), were most frequently the locus of discrepancies in the columnar consistency of
center-surround properties (Fig. 8). The
discrepancies were determined by comparing the sign of the SI of each
unit with the prevailing sign for the penetration as a whole. It is
noteworthy, however, that in layer 4, the discrepant units accounted
for less than a quarter of the total recorded there. While
discrepancies were more frequent in layer 6A (nearly 50%), this layer
is probably too thin to be resolved in any of the 2dg sections (each
40-µm thick). It may account, however, for some of the decrease in
contrast seen in the lower layers (Fig. 7D).
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Relationship between center and surround
The surround direction test was used to compare the preferred directions of the center and surround. Occasionally neurons were encountered whose optimal stimulus consisted of a surround moving perpendicular to the center (shearing type motion); however, the strong overall tendency was for the surround to be maximally excitatory when it was moving in either the same or the opposite direction to that of the center (Fig. 9A). From the Gaussian fit to the surround direction tuning curve, a measure of the sharpness of direction tuning for the surround (Fig. 9B) was also obtained. Quantitative direction tuning for the centers was performed on only a subset of these neurons (Fig. 9C), but it was quite clear that the centers were more sharply tuned for direction than were the surrounds (mean tuning bandwidth of center = 105°; surrounds = 127°; P = 0.0034, Mann-Whitney U test).
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On a subset of neurons, tests were performed to look for interactions
between the tuning of centers and surrounds for both speed (Fig.
10) and direction (Fig.
11). These tests
consisted of multiple measurements of the tuning of the center in the
presence of surrounds moving at different speeds or in different
directions. All of the different combinations of center and surround
motion were randomly interleaved in one large block of trials. The
results for relative speed tuning of a single neuron are shown in Fig. 10C. The preferred speed of the center was approximately
4°/s, regardless of the speed with which the surround moved. The
overall responsiveness of the neuron was, however, modulated by the
surround motion. This was true for the nine neurons tested
quantitatively (Fig. 10E)the shifts of the peak of the
speed tuning curve induced by surround motion were clustered around
zero, suggesting independent speed tuning for center and surround. For
the pooled data, neither the slope nor the y-intercept of
the regression line was significantly different from 0 (P > 0.10). An analogous set of measurements was made
for direction tuning (Fig. 11). The results were similar in that the
peak of the direction tuning curve was not shifted significantly by
changes in the direction of the surround although the overall level of
responsiveness was modulated by surrounds of different directions (Fig.
11C). This basic result was true for the three neurons
tested quantitatively (Fig. 11E), and it was obvious for a
much larger number of cells tested qualitatively.
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Complex motion contrast
A subset of neurons in the interbands had RFs that could not be
described as simply center-surround. Like nearly all interband cells,
they responded best to bars or to small fields of random dots. They
differed, however, in that an optimally sized random dot patch elicited
a strong response over a rather large area of the visual field. This
first became evident when the size of the CRF was superimposed on the
ASC (Figs. 12A and 13). For
such neurons the optimal random dot patch diameter was actually much smaller than the CRF. The optimally sized random dot patch
(~1.5° in the example of Fig. 12B) could elicit an
excitatory response over a much larger region of the visual field
(approximately 4 × 4°). Note, however, that if this 4 × 4° region of the visual field was covered with an equal-sized patch
of random dots, the neuron's response was barely above baseline (Fig.
12A). RFs of this type appear to generalize the property of
surround antagonismor motion contrast
across retinotopic space.
Because this process seems analogous to the operation performed by
complex cells with respect to orientation (Hubel and Wiesel
1962
) and by complex unoriented cells with respect to chromatic
opponency (Hubel and Livingstone 1985
), this property
was termed "complex."
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Once the existence of the complex RF was clear, it was found in 24 single units of 140 sites mapped (17%). The ASCs, along with the border of the CRF, are shown for a randomly chosen subset of nine of these in Fig. 13. It was obviously important to document this property for single units because a multi-unit response of this type might only indicate a group of neurons with simple center-surround antagonism but slightly offset RFs. Although the incidence of complex motion contrast seems rather low, neurons exhibiting it also tended to cluster, not only columnarly, within interbands, but within specific layers as well (Fig. 14). In this penetration six single units (marked by *) had RFs of the complex motion contrast type: three in layer 3B (the lowermost part of supragranular cortex containing distinctive large pyramidal neurons) and three in layer 5. Of the 24 complex motion contrast neurons, 14 were recorded in layer 3B, 10 were recorded in layer 5, and none were outside of these two layers. These facts combine to make for local densities that may be quite high. Of the 140 sites referred to above, approximately half were in bands and another quarter were outside of layers 3B and 5. If only neurons in interbands within layers 3B and 5 were considered, then complex motion contrast cells accounted for 24 of 42 (57%) of the recordings.
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DISCUSSION |
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A survey of center-surround interactions within the RFs of neurons in owl monkey MT revealed two basic categories: neurons with antagonistic surrounds that responded optimally to discrete objects, such as bars, and were insensitive to wide-field motion and neurons with reinforcing surrounds that responded best to wide-field motion of textures. These types were clustered together and organized anatomically into columnar slabs that could be observed directly as dark bands and light interbands, using 2dg functional labeling. For individual neurons, the preferred direction for the surrounds, with respect to that of the centers, tended to be in either the same or the opposite direction, and the direction tuning of the surrounds was broader, on average, than that of the centers. The general effect of the surrounds was not to shift the tuning of the center for either direction or speed but rather to modulate the overall responsiveness of the neuron. Finally, a RF that generalized the property of surround antagonism over retinotopic space, named "complex motion contrast," was found in layers 3B and 5 of the interbands.
Functional organization for what?
The sine qua non of MT neurons with antagonistic surrounds is that
they do not respond to wide-field motion. Thus it is plausible that the
clustering of center-surround properties would produce the
band-interband patterns observed in the 2dg experiments. Another possible explanation for these patterns, however, is an organization for binocular disparity such as that described in the macaque (DeAngelis and Newsome 1999). This organization consists
of columnar clusters of neurons that are nonselective for binocular
disparity interdigitated with zones containing systematic maps of
columns of neurons preferring different disparities. Given such an
organization, a wide-field motion stimulus might also produce patchy,
columnar 2dg uptake, because the nonselective zones would be more
active than those selective for a particular disparity. Even the
experiments during which binocular disparity was varied over the course
of the 2dg infusion would not rule out the contribution of such an organization because any given neuron within the disparity-selective zones would still be active a smaller percentage of the time. Based on
the present results, however, it appears unlikely that a similar
organization for binocular disparity exists in the owl monkey: neurons
were always tested for sensitivity to binocular disparity, albeit
qualitatively, and selectivity was only rarely found. For
disparity-selective neurons, the stimulus was always presented at the
optimal center disparity when performing tests of center-surround
interactions. Thus differences in disparity tuning cannot account for
the 2dg results in the owl monkey.
Another point worth noting is that it was difficult to find a single quantifiable parameter that adequately captured the functional organization. The ASC provided a good measure for some neurons, but it was not useful for neurons that did not respond to random dots at all (see Fig. 3). These "bar" cells were encountered very frequently within the interbands. Although an antagonistic surround could usually be demonstrated by stimulating the CRF with a bar while stimulating the surround with an annulus of random dots, it was difficult to compare this test with the ASC data. This feature undoubtedly diluted the statistical analysis of periodic organization; however, it actually strengthens the argument that the interbands are more specialized for processing object-based motion (see following text). Thus there appear to be at least two properties that distinguish the different regions labeled by 2dg: a change in the nature of the center-surround interactions, from reinforcing to antagonistic, and a change in the nature of the optimal stimulus, from more texture-like to more object-like.
Further support for the functional segregation reported here comes from
a recent anatomical study where it was found that the connections of MT
neurons are also segregated (Berezovskii and Born 2000).
When retrograde tracers were injected into the dorsal subregion of the
fundus of the superior temporal sulcus (FSTd) and MST, the
labeled neurons in MT were generally restricted to either the bands or
the interbands. This result both strengthens the idea that they
represent different functional compartments and suggests that the
distinction between wide-field and local motion processing continues at
subsequent cortical stages. The previously demonstrated physiological
grouping of neurons responding preferentially to local or wide-field
motion in macaque area MST (Eifuku and Wurtz 1998
;
Komatsu and Wurtz 1988
; Tanaka et al. 1986
) indicates that a similar pattern may occur in old world monkeys as well.
Model of owl monkey MT
These observations on the grouping of motion-processing neurons
whose RFs possess different types of spatial interactions, combined
with the previously described organization for preferred direction
(Malonek et al. 1994), suggest a modular organization of
owl monkey MT analogous to that proposed for macaque striate cortex by
Hubel and Wiesel (1977)
. In this model (Fig.
15), direction columns occupy one
dimension and occur at a spatial scale similar to that of orientation
columns in striate cortex. The band-interband organization, comprising
a second dimension, is rather coarser, similar to that for ocular
dominance columns in striate cortex. The purpose in putting forth such
a geometrically simple model is not to suggest that these two stimulus
dimensions are represented at right angles in the cortex. The actual
geometry is undoubtedly more complex
again, by analogy with the
relationships observed in striate cortex (Blasdel 1992
;
Obermayer and Blasdel 1993
)
and may be more correctly
described as a "polymap" than as strictly "modular"
(Swindale 1990
). The model merely serves to emphasize that both representations are relatively orderly and columnar, that
they occur at different spatial scales, and that they are presumably
not strictly parallel, since this would lead to coverage problems.
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Functional implications
Motion of images on the retina can occur either because something
in the world is moving or because the retina is moving (due to eye,
head, or body motion on the part of the observer). Because both types
of motion usually occur together, disambiguating them is a difficult
and important task for the motion systemimportant because they convey
different kinds of information and generally call for different motor
responses on the part of the animal. This has been shown most clearly
in the visual system of the fly, which also appears to anatomically
segregate wide-field and local-contrast motion processing neurons
(Egelhaaf et al. 1988
). Retinal motion caused by
observer motion is necessarily wide-field and largely coherent, at
least at the spatial scale of MT RFs
stimulus conditions during which
only the band cells are providing useful motion signals. Interband
cells, on the other hand, seem best suited to convey information about
objects: either actual motion of an object or motion discontinuities in
the flow field created by objects at different distances from the
observer as he moves through the environment (Gibson
1950
). A functional clustering of these different signals would
seem to make sense, then, since they are qualitatively different in
their meaning to the organism.
Recent microstimulation experiments in macaque MT support this notion
of a functional dichotomy (Born et al. 2000). Different physiologically identified regions of MT were stimulated while the
monkeys performed a step-ramp visual tracking task, and the directional
effects on smooth pursuit eye movements were measured. When regions
that were more interband-like (i.e., those preferring local motion
contrast) were stimulated, effects were seen in the preferred direction
of the neurons stimulated. When band-like regions (i.e., those
responsive to WF motion) were stimulated, the effects tended to be in
the opposite direction
as if the microstimulation signal
was interpreted as background motion in the preferred
direction that induced a target-associated signal in the opposite
direction (Duncker 1929
).
Relationship between center and surround
Detailed tests on single units revealed that the center and
surround behaved quite independently. Changes in the speed or direction
of the surround did not induce shifts in the tuning of the center as
one might expect if only relative velocity were being
represented (Frost and Nakayama 1983). This does not
mean, however, that relative velocity information cannot be extracted from the signals of interband neurons. Modeling studies have shown that
an overall modulation of the type described here can be used to compute
a truly relative signal. For example, the eye-position modulation of
the retinotopic responses of neurons in posterior parietal cortex
(Andersen et al. 1985
, 1987
) can be readily converted to
a craniocentric representation of the visual world (Zipser and
Andersen 1988
). It seems entirely plausible that the sort of
surround-modulated responses reported here might be similarly transformed to provide the true relative velocity of an object with
respect to the visual background.
Complex motion contrast
The RFs of a subset of neurons in the interbands extend the
property of motion surround antagonism over a larger region of the
visual field. This type of RF has not been described previously in MT
of either the owl monkey or the macaque, although something very
similar has been described in macaque MSTl (Tanaka et al. 1986), in neurons classified as "figure type." Once sought
out, this RF type proved to be quite common in owl monkey MT, and the neurons embodying it showed a high degree of topographic and laminar specificity.
The basic operation at the heart of complex motion contrastthat of
taking a RF property and generalizing it over retinotopic space
appears to be quite prevalent. It has been reported in a number
of other cell types, processing different visual modalities, recorded
in different regions of the visual cortex: "complex cells" in
striate cortex, with respect to orientation selectivity (Hubel and Wiesel 1962
); "complex unoriented cells" in V2, with
respect to chromatic and spatial opponency (Hubel and
Livingstone 1985
); "higher order hypercomplex cells" in cat
area 19 (Hubel and Wiesel 1965
) and monkey V4
(Desimone and Schein 1987
), with respect to end-stopping; and, quite possibly, "vector field" cells in MST, with respect to optic flow (Duffy and Wurtz 1991
).
As previously suggested by Hubel and Wiesel (1962), this
type of RF may be realized by a very generic type of circuit, which might be constructed by "or-gating" together inputs from many neurons with simple antagonistic surrounds for moving stimuli. Because
of the surround inhibition in the input cells, the complex cell behaves
more like an exclusive "or" gate: two small patches of
motion are less effective than one, presumably because the second patch
impinges on the surrounds of neurons excited by the first patch (and
vice versa) thus less effectively driving any of the input cells.
Finally, the existence of the simple and complex types of
motion-contrast neurons represents another example of a general tendency in hierarchical processing, first noted by Barlow
(1993), to alternate RFs that are more selective
than their predecessors along some stimulus dimension with those that
are less selective. In this case, the simple type of
antagonistic RF is more selective than previous motion processing RFs
by virtue of its antagonistic surround. It responds only to motion
contrast. The complex version, while retaining the
requirement for contrast, is less selective in terms of the exact
retinotopic position of the stimulus. The purpose of this alternation
remains mysterious; however, its repeated appearance may indicate that
the cerebral cortex is relatively computationally homogeneous. It will
be interesting to see if these trends continue further along the visual
pathways and whether evidence for similar kinds of circuitry will be
found in higher-level association cortex as well.
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ACKNOWLEDGMENTS |
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I am grateful to R. Tootell for advice and support during early stages of this work. E. Kaufman provided excellent technical assistance. D. Hubel and C. Pack made helpful comments on the manuscript.
This work was supported by National Institutes of Health Grants EY-11379, EY-12196, and RR-00168 and by a grant from the Klingenstein Foundation.
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FOOTNOTES |
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Address for reprint requests: Dept. of Neurobiology, Harvard Medical School, 220 Longwood Ave., Boston, MA 02115-5701 (E-mail: rborn{at}hms.harvard.edu).
Received 7 December 1999; accepted in final form 6 July 2000.
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REFERENCES |
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