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The Journal of Neuroscience, October 1, 2002, 22(19):8633-8646
Circuits for Local and Global Signal Integration in Primary
Visual Cortex
Alessandra
Angelucci1,
Jonathan B.
Levitt2,
Emma
J. S.
Walton3,
Jean-Michel
Hupé4,
Jean
Bullier4, and
Jennifer S.
Lund1
1 Department of Ophthalmology and Visual Science, Moran
Eye Center, University of Utah, Salt Lake City, Utah 84132, 2 Department of Biology, City College of the City
University of New York, New York, New York 10031, 3 Department of Visual Sciences, Institute of
Ophthalmology, University College London, London EC1V 9EL, United
Kingdom, and 4 Centre de Recherche Cerveau et Cognition,
Centre National de la Recherche Scientifique-Unité Propre de
Recherche Unité Mixte de Recherche 5549, Université
Paul Sabatier, Toulouse 31062, France
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ABSTRACT |
Contrast-dependent changes in spatial summation and contextual
modulation of primary visual cortex (V1) neuron responses to stimulation of their receptive field reveal long-distance integration of visual signals within V1, well beyond the classical receptive field
(cRF) of single neurons. To identify the cortical circuits mediating
these long-distance computations, we have used a combination of
anatomical and physiological recording methods to determine the spatial
scale and retinotopic logic of intra-areal V1 horizontal connections
and inter-areal feedback connections to V1. We have then compared the
spatial scales of these connectional systems to the spatial dimensions
of the cRF, spatial summation field (SF), and modulatory surround field
of macaque V1 neurons. We find that monosynaptic horizontal connections
within area V1 are of an appropriate spatial scale to mediate
interactions within the SF of V1 neurons and to underlie
contrast-dependent changes in SF size. Contrary to common beliefs,
these connections cannot fully account for the dimensions of the
surround field. The spatial scale of feedback circuits from
extrastriate cortex to V1 is, instead, commensurate with the full
spatial range of center-surround interactions. Thus these connections
could represent an anatomical substrate for contextual modulation and
global-to-local integration of visual signals. Feedback projections
connect corresponding and equal-sized regions of the visual field in
striate and extrastriate cortices and cover anisotropic parts of visual
space, unlike V1 horizontal connections that are isotropic in the
macaque. V1 isotropic connectivity demonstrates that anisotropic
horizontal connections are not necessary to generate orientation
selectivity. Anisotropic feedback connections may play a role in
contour completion.
Key words:
primary visual cortex; extrastriate cortex; feedback
connections; lateral connections; surround modulation; macaque
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INTRODUCTION |
A central question in visual
cortical processing is how local signals are integrated across space to
generate global percepts. Traditionally, visual information has been
seen as ascending through a hierarchy of cortical areas, with cells at
each successive stage processing inputs from increasingly larger
regions of space. However, long-distance integration of visual signals
can occur at very early stages of processing. The response of cells in
the primary visual cortex (V1) to stimulation of their receptive field
(RF) can be modulated in a selective way by contextual stimuli lying far outside the RF in the RF surround (Blakemore and Tobin 1972 ; Nelson
and Frost, 1978; Allman et al., 1985; Gilbert and Wiesel, 1990; Levitt
and Lund, 1997; Walker et al., 1999). Furthermore, V1 RFs show dynamic
spatial properties, changing in size depending on stimulus contrast
(Kapadia et al., 1999; Sceniak et al., 1999). These neurophysiological
responses require integration of visual signals beyond the RF of single
V1 neurons and thus cannot be easily explained by classical RF
concepts. Identifying the neural circuitry underlying these
long-distance computations is crucial, because they may represent the
neural substrates for feature grouping (Kapadia et al., 1995; Mizobe et
al., 2001) and figure-ground segregation (Knierim and Van Essen, 1992;
Nothdurft et al., 1999).
Currently, most models of center-surround interaction in V1 are based
on intrinsic horizontal (or lateral) connections (Gilbert et al., 1996;
Somers et al., 2002). These are long-range, reciprocal, intralaminar
projections made by excitatory neurons in layers 2/3, 4B/upper 4C ,
and 5/6 of macaque area V1 (Rockland and Lund, 1983). These connections
show a periodic, patchy pattern of termination and preferentially link
cortical domains of similar functional properties (Malach et al., 1993;
Yoshioka et al., 1996). On the basis of laminar origin and termination,
connections between visual cortical areas have been classified as
feedforward (FF) or feedback (FB), and a hierarchical organization of
cortical areas has been proposed previously (Rockland and Pandya, 1979;
Felleman and Van Essen, 1991). V1, at the bottom of the hierarchy,
receives its main FF inputs from the thalamus and sends partially
segregated FF projections to several extrastriate cortical areas,
which, in turn, send FB projections to V1. It has been suggested that FB connections have a less precise retinotopic organization than FF
projections (Perkel et al., 1986; Salin and Bullier, 1995), and that
only FF inputs can drive V1 neurons, whereas FB connections would have
a modulatory influence (Crick and Koch, 1998). FB connections may
therefore represent an additional or alternative substrate for
contextual modulation in V1.
The aim of this study was to provide a basis for disentangling the
relative roles of inter-areal FB and intra-areal horizontal connections
in integrating signals within and beyond the RF of V1 neurons. We
reasoned that to mediate interactions within or beyond the RF, a given
connectional system must be commensurate with the spatial extent of the
RF or modulatory surround field of the neuron. Thus, we have compared
the visuotopic scale of each connectional system with the spatial
extent of the classical RF, spatial summation field (SF), and
modulatory surround field of macaque V1 neurons. Our results
demonstrate that monosynaptic V1 horizontal connections are of an
appropriate scale to mediate interactions within the SF and could
represent an anatomical substrate for dynamic changes in SF size such
as induced by stimulus contrast or scotomata (Das and Gilbert, 1995).
FB circuits from extrastriate cortex to V1, on the other hand, are of
an appropriate scale to play an important role in global integration of
visual signals and modulation of responses far beyond the SF of V1 cells.
Parts of this work have been published previously in abstract form
(Angelucci et al., 1998, 2000).
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MATERIALS AND METHODS |
Electrophysiological recording. In a first set of
animals, quantitative electrophysiological recording terminal
experiments were performed on seven adult macaque monkeys (Macaca
fascicularis or M. mulatta). All procedures conformed
to British Home Office and United States National Institute of Health
guidelines. Animals were premedicated with atropine sulfate (0.02-0.04
mg/kg) and acepromazine maleate (0.05 mg/kg) and preanesthetized with
ketamine (10-30 mg/kg, i.m.). The trachea and saphenous veins were
cannulated; the animal was artificially ventilated with room air or
with a 50:50 mixture of O2 and
N2O; and anesthesia was maintained by continuous
intravenous infusion of sufentanil citrate (4-8
µg · kg 1 · hr1).
The animal's head was fixed to a stereotaxic apparatus; a small craniotomy and durotomy were made over the occipital cortex; and a
tungsten-in-glass microelectrode (Merril and Ainsworth, 1972) was
positioned over the exposed cortex, which was then covered with warm
agar. To minimize eye movements, on completion of surgery, the animal
was paralyzed by continuous intravenous infusion of vecuronium bromide
(0.1 mg · kg1 · hr1)
in lactated Ringer's solution with glucose (5.4 ml/hr).
Electroencephalogram and electrocardiogram were monitored continuously.
Peak expired CO2 was maintained near 4.0%,
rectal temperature near 37°C, and blood oxygenation near 100%.
The pupils were dilated and accommodation paralyzed with topical
atropine; the corneas were protected with zero power rigid gas-permeable contact lenses; and the eyes were refracted. The location
of the foveas was plotted (and checked periodically throughout the
experiment) on a tangent screen using a reversible ophthalmoscope. Extracellular recordings were made in the opercular region of area V1
between 2 and 8° retinal eccentricity in the lower visual field.
Spikes were conventionally amplified and displayed and stored on a
personal computer (resolution, 250 µsec). Small electrolytic lesions
(1-2 µA for 2-5 sec) were made along the electrode track and later
reconstructed on Nissl- and cytochrome oxidase (CO)-stained tissue
sections. For quantitative studies, visual stimuli were displayed on a
Barco ICD 451B color TV monitor driven by an AT Truevision Vista
Graphics board. At a viewing distance of 114 cm, the screen subtended
13 × 13° of visual angle. Stimuli consisted of square patches
of drifting achromatic sinusoidal gratings of average luminance of 37.5 cd/m2. Contrast was held fixed at 75%
(i.e., below response saturation for most cells).
The location and size of the classical RF or minimum response field
(mrf; Barlow et al., 1967) of the neuron were initially hand-mapped
through the dominant eye; this was then confirmed by computer mapping.
All subsequent quantitative experiments proceeded under computer
control. The preferred orientation, direction of motion, spatial and
temporal frequency, and size of stimuli of the neuron were determined.
The optimal parameters for the recorded cell were then used to measure
RF and surround sizes. Stimuli were presented for 2-4 sec within each
block of trials in a randomized order, and results of four to eight
repeated blocks were averaged. To measure the spontaneous firing rate
of the cell, interleaved blanks of the same mean luminance as the
stimuli were presented. To spatial summation data we fit functions
representing a difference of the integrals of excitatory and inhibitory
Gaussian mechanisms (Sceniak et al., 2001) as described in detail by
Levitt and Lund (2002). From these functions we determined the stimulus
diameter at which responses peaked and asymptoted. Population values
are expressed as mean ± SEM. Statistical significance of laminar
variation was tested with the Kruskal-Wallis test.
Combined tracer injections and physiological recording. In a
separate set of animals, combined anatomical and electrophysiological recording survival experiments were performed on nine adult macaque monkeys (M. fascicularis or M. mulatta). Tracer injections (n = 17, all
clearly confined to the cortical gray matter) were made in
electrophysiologically characterized cortical loci between 2.2 and
7.5° eccentricity in the lower visual field representation of areas
V1, V2, or V3. The animals were prepared as described above, intubated,
and anesthetized with 0.5-2% isoflurane in a 70:30 mixture of
N2O and O2 (three animals
were anesthetized with Sufentanil as described above). Fluids (lactated
Ringer's solution at 1-2
ml · kg1 · hr1)
were continuously infused intravenously to support cardiovascular function. Monitoring of vital signs, surgery, recordings, and hand
plotting of RFs were performed as described above. A short-duration topical mydriatic agent (cyclopentolate) was applied to the corneas, and the eyes were fitted with contact lenses.
Areas V2 and V3 were identified electrophysiologically using the known
sequence of gray-white matter transitions as described previously
(Gegenfurtner et al., 1997). Corresponding retinotopic loci in V1 and
V2 were identified in three animals as described by Hupé et al.
(2001b). Once the appropriate cortical sites were found, the position
of the microelectrode was recorded, the electrode was withdrawn, and
the animal was paralyzed by intravenous infusion of vecuronium bromide
(0.1 mg · kg1 · hr1,
with a loading dose of 1 hr). The foveas were plotted, and a foveal mrf
was mapped in V1 (and periodically throughout the experiment) to
monitor eye movements. A recording electrode glued to a glass micropipette (intertip distance, <50 µm; Hupé et al., 1999)
filled with a tracer solution was lowered into the same striate or
extrastriate locus where the initial recordings were performed.
RF size and eccentricity of cells through the depth of the penetration
were first remapped, and then the tracer was injected through the
attached pipette (inner tip diameter, 13-17 µm). The tracers used
were cholera toxin subunit B [CTB, low salt; List Biologic, Campbell, CA; 1% in 0.1 M phosphate buffer (PB), pH 6.0] or
biotinylated dextran amine (BDA, MW 3000; Molecular Probes, Eugene, OR;
10% in 0.01 M PB, pH 7.25). The tracers were
delivered iontophoretically using 2 µA for CTB and 6 µA for BDA of
positive current in 7 sec on-off cycles for 10-30 min. CTB was
preferred for these studies, because its sensitive anterograde and
retrograde transport reveals reciprocal connections to an injected
point (Angelucci et al., 1996). However, in some cases BDA was used to
compare the extent of the label with CTB. At the end of the injection,
to avoid leakage of tracer along the pipette track, the pipette was
left in place for at least 30 min and then withdrawn while reversing
the current to negative. In five V1 and three V2 injection cases
(n = 4 animals), after the tracer injection in
physiologically characterized loci, additional recordings were made of
RF size and location along a few electrode penetrations made at 1 mm
intervals around the injection site; recording sites were marked by
electrolytic lesions. In all remaining cases (n = 5 V1
and 4 V3 injections) recordings were made only at the injection site;
retinotopic maps in these cases could not be recorded because of lack
of time and need to recover the animal. The animal was recovered from
paralysis and anesthesia, allowed to survive for 10-20 d, and finally
killed with an overdose of sodium pentobarbital (100 mg/kg, i.v.) and perfused transcardially with saline followed by 4% paraformaldehyde in
0.1 M PB, pH 7.4, for 30 min.
Areas V1 and V2 were dissected free, flattened between glass slides,
postfixed overnight, cryoprotected by sinking in 30% phosphate-buffered sucrose, and finally sectioned on a freezing microtome at 40 µm tangentially to the pial surface. The block containing areas V3 and MT was similarly postfixed and
cryoprotected, and then cut parasagittally. CTB was revealed
immunohistochemically using the protocol of Angelucci et al. (1996);
BDA was revealed using standard Vector Laboratories (Burlingame, CA)
ABC VIP-based reactions. Some (n = 3) animals
received an injection of CTB and one of BDA in corresponding
retinotopic loci in areas V1 and V2. In these brains, CTB was revealed
using a standard peroxidase-antiperoxidase method (Lanciego et al.,
1998). To reveal areal and layer boundaries, interleaved sections were
stained for CO (one in three sections of tissue containing areas V1 and
V2) or for myelin (Gallyas, 1979) or Nissl substance (one in five
sections, for each method, of tissue containing V3 and MT).
Data analysis. CTB and BDA anterograde and retrograde labels
were mapped in each available section using a camera lucida. Layer
boundaries were identified and drawn by overlaying the maps of the
label to adjacent CO- or Nissl-stained sections. Areal boundaries were
identified using the pattern of CO staining (for V1 and V2) or Gallyas
staining (for V3 and MT) as well as the specific pattern of anterograde
and retrograde label. Surface-view two-dimensional (2D) composite
reconstructions of the label were made separately for each V1 and V2
layer by overlaying maps of serial tangential sections using vascular
landmarks as alignment points. Surface-view reconstructions of the
label in V3 and MT were made from serial sagittal sections as described
in detail previously (Johnson et al., 1989). Briefly, the mapped label
in each section was projected onto a line running through midlayer 4, using a radial segmentation scheme, and serial sections were aligned
using a combination of sulcal and vascular landmarks. Cells were
counted, and plots of label density were computer-generated. Typically,
label density showed a Gaussian-like distribution. Our definition
of a labeled field included all bins with label density within 95% of
the peak density (see Fig. 4). For eight injections (five in V1 and
three in V2), the density maps of the V1 and V2 label were overlaid to
physiological maps obtained from the same animal in these two cortical
areas, using the location of electrolytic lesions as alignment points;
the visuotopic extent of the labeled fields was measured directly on
the retinotopic maps as well as estimated as described below.
In all remaining cases (n = 5 V1 and 4 V3 injection
cases) in which retinotopic maps were not recorded, the visuotopic
extent of labeled connectional fields was estimated as follows. All
labeled fields in striate and extrastriate cortex were anisotropic in cortical space their long axis corresponding to the cortical area elevation axis, and to the axis of anisotropy of the magnification factor (MF), demonstrated at least for V1 (where it runs parallel to
the vertical meridian; Van Essen et al., 1984; Tootell et al., 1988;
Blasdel and Campbell, 2001) and V2 (where it runs orthogonal to the CO
stripes; Roe and Ts'o, 1995). We measured the density map of each
labeled field along (elevation axis) and across (azimuth axis) the
representation of the isopolar lines of the visual field, using as a
reference published retinotopic maps of striate cortex (Van Essen et
al., 1984; Dow et al., 1985; Tootell et al., 1988) and extrastriate
cortex [V2 (Gattas et al., 1981; Roe and Ts'o, 1995), V3 (Burkhalter
et al., 1986; Gattas et al., 1988), and MT (Albright and Desimone,
1987; Maunsell and Van Essen, 1987)]. Cortical measurements were
corrected for tissue shrinkage caused by histological processing. This
was estimated on a case-by-case basis for 12 of 17 injections using the
measured in vivo distance between electrolytic lesions,
between injection sites, or both. In our hands, shrinkage caused by CTB
and BDA processing ranged in different cases between 30-33 and
8-13%, respectively. We also estimated shrinkage caused by perfusion
and cryoprotection (~12%) and applied this correction factor to the
intersection distance, i.e., to the anteroposterior dimension of the 2D
maps obtained from serial sagittal section reconstructions (see Fig.
4). For five injections in which shrinkage could not be estimated
directly, we applied a 30% shrinkage correction for CTB and 10% for
BDA (a possible 2-3% error in shrinkage correction in these cases would not have affected our results). Knowing the cortical extent of
labeled fields and the eccentricity of injection sites (recorded in all
cases), to estimate the visuotopic extent of the two axes of label, we
used published equations relating MF and scatter (S) in RF center position to retinal eccentricity in
areas V1-V5. For labeled fields within V1, we used equations from Van
Essen et al. (1984) and Tootell et al. (1988), because these authors measured MF separately along and across the isopolar axis of
V1. Because MF and S are constant along
isoeccentricity contours, the linear visuotopic extent (designated
D°) (Fig. 1a) of
the axis of the labeled field along these contours was estimated as:
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(1)
|
where D(mm) (Fig.
1b) is the measured length (in millimeters) of the labeled
field along the isoeccentricity axis, and S was estimated at
the injection eccentricity using the equation from Dow et al. (1981).
Because retinal eccentricity (E), and thus
MF and S, vary along the isopolar axis, we
determined the retinotopic location of the end points of this axis of
label, denoted as E+ and
E, respectively (Fig. 1a;
with E+ > E) by
integrating the equations (Van Essen et al., 1984; Tootell et al.,
1988) relating MF to E along the isopolar axis of
V1. Thus, for example, integrating equation
MF(E) = aEb mm/°, from Van Essen et
al. (1984), it follows that:
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(2)
|
where a and b are constants,
Ec is the physiologically recorded
eccentricity (in degrees) of the injection site or of the center of the
long axis of the label (Fig. 1a), and
 X+ and X are the measured cortical
separation (in millimeters) of the two end points
(X+ and
X) from the center, Xc (Fig. 1b).
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Figure 1.
Estimated extent of corticocortical connectional
fields in visual field coordinates. a, Visual field
measurements. VM, HM, Vertical and horizontal meridian,
respectively. Ec, Retinal eccentricity
of the center of the injection site or of the labeled field determined
experimentally for all cases by electrophysiological recording.
E+, E,
estimated retinal eccentricity of RF center of cells at the end points
of the axis of the labeled field (see Eq. 2). Dashed
circles, Mean RF size of neurons at the eccentricity of the end
points of the labeled field, measured experimentally in the same or
different animals. D°, estimated linear visuotopic
extent of the axis of the labeled field (gray circle
diameter). ARF, Aggregate receptive field size
of the labeled field's axis, calculated as D° + mean
RF size of cells at the end points of the labeled field.
b, Cortical measurements.
Xc, Cortical location of the injection
site or of the center of the labeled field.
X+, X,
Cortical location of cells at the end points of the labeled field's
axis. X+,
X, Measured cortical distance of the
end points of the labeled field from the center.
D(mm), Measured cortical extent of the
axis of the labeled field (gray oval
diameter).
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The linear visuotopic extent (D°) for the long axis of
label is then given by:
|
(3)
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The aggregate receptive field size (ARF) (Fig. 1a) was
calculated as:
|
(4)
|
where mRF is the mean RF size of cells at the end
points of the axis of label, and can reflect the mrf or summation field of the neurons (see Results). We used our own physiological measures of
RF sizes appropriate for the end points eccentricity and cortical layer
location. These were measured either in the same animal in which the
tracer injection was made or in a separate set of quantitative
physiological experiments performed in different animals (see above).
Below we provide a detailed example of our estimates of the visuotopic
extent of the injection site and resulting labeled horizontal
connections for the case in Figure 6a. The V1 injection was
made at 6.5° eccentricity in the lower visual field, 4° from the
vertical meridian. D° along the anteroposterior (AP; i.e., isoeccentricity) axis of V1 was estimated substituting in Equation 1
the following values: D(mm) = 1.13 mm
(measured cortical extent of injection site AP axis) or 4.34 mm
(measured cortical extent of horizontal connections AP axis);
MF (at E = 6.5°) = 1.3 mm/° (using
equation MF = 13E1.22 mm/°; Van Essen et
al., 1984); and S (at E = 6.5°) = 0.16° (using equation S = 0.314 × mrf size  0.86 min; Dow et al., 1981).
D° of the injection site and resulting horizontal
connections along the mediolateral (ML; i.e., isopolar) axis of V1 was
estimated substituting in Equations 2 and 3 the following values:
a and b = 11.7 and 1.01 (constants from
equation MF = 11.7E1.01 mm/°; Van Essen
et al., 1984); Ec = 6.5°
(physiologically recorded E of injection site);
X+ and
X (for injection site) = 0.55 mm (measured cortical extent of injection site ML radius); X+ and
X (for horizontal
connections) = 2.1 and 3.1 mm (measured cortical separation of
furthest medial and lateral labeled points, respectively, from the
injection center); and S (at E = 6.5°) = 0.16°.
From Equation 2 we obtained E+ and
E (for injection site) = 6.8 and 6.2°, and E+ and
E (for horizontal connections) = 7.8 and 4.97°. From Equations 1 and 3 we obtained D°
(for injection site) = 1.03° (AP axis) × 0.78° (ML
axis), and D° (for horizontal connections) = 3.5°
(AP axis) × 3° (ML axis).
The ARF size of the V1 injection site in Figure 6a was
calculated as follows: ARF of AP axis = D° of
injection (1.03°) + mean RF size in V1 layer 2/3 at 6.5°
eccentricity [mrf = 0.55°; high- and low-contrast
summation field (SF) = 1.15 and 2.65°,
respectively]. ARF of ML axis = D° of injection
(0.78°) + mean RF size/2 in V1 layers 2/3 at
E+ (6.8°) eccentricity
(mrf = 0.56°; high- and low-contrast
SF = 1.18 and 2.7°, respectively) + mean RF size/2 in
V1 layers 2/3 at E (6.2°)
eccentricity (mrf = 0.54°; high and low contrast
SF = 1.13° and 2.6°, respectively). RF sizes in this case were
obtained from our own equations relating RF size to eccentricity in the
different layers of V1 and derived from a separate set of quantitative
physiological experiments (see above).
The above estimates were obtained using MF values from Van Essen et al.
(1984). Although MF values reported by Tootell et al. (1988) and
Blasdel and Campbell (2001) tend to be slightly larger than those of
Van Essen et al (1984), applying MF values from these other authors to
the above estimates yielded only slightly smaller values of
D° and ARF size. Thus, for example, the aggregate high-contrast SF size of the V1 injection (along the ML axis) in Figure
6a measured 1.9° using the MF of Van Essen et al. (1984) but was 1.8° using the MF of Tootell et al. (1988). The ratio of
D° of lateral connections to the aggregate high-contrast
SF size of the V1 injection was 1.6 (for the ML axis) using the MF from
Van Essen et al. (1984) and 1.3 using the MF from Tootell et al.
(1988). Thus, using MFs in the literature from different authors, we
observed minimal differences in our estimates.
For labeled fields within the central 5° of V2, we used MF and S
values from Roe and Ts'o (1995), because they reported separate measures of MF along and across CO stripes. Published measurements of
MF in more peripheral V2 (Gattas et al., 1981) and in V3 (Gattas et
al., 1988) and MT (Albright and Desimone, 1987; Maunsell and Van Essen,
1987) are averaged across isopolar and isoeccentricity axes, thus not
taking into account possible anisotropies in MF. Similar to V1 and V2,
anatomical anisotropies of labeled connectional fields in areas V3 and
MT likely reflect anisotropies in MF within these areas. Thus, for the
label in more peripheral (>5°) V2 and for all labeled fields in V3
and MT, we estimated D° only for the long axis of the
label field, substituting in Equation 1 the largest published values of
MF (Gattas et al., 1981; Albright and Desimone, 1987; Gattas et al.,
1988) at the retinal eccentricity of the injection site. The rationale
for this choice was that the largest values of MF at a given retinal
eccentricity most likely reflect MF values along the anisotropy axis.
Using the largest values of MF might have caused us to underestimate
the extent of retrogradely labeled FB fields in visual field
coordinates. This error would not have altered our conclusions that the
visuotopic extent of FB fields is larger than that of V1 intrinsic
horizontal connections. To avoid introducing additional errors, we did
not attempt to estimate the visuotopic extent of FB fields along their shorter axis or their visual field anisotropy; thus, the retrogradely labeled fields of cells of origin of FB connections in extrastriate cortex are represented in visual space as circles (see Fig.
7a) rather than ovals (as are the fields of V1 horizontal
connections, or of terminal FB connections inV1) (see Figs.
6a, 7a, 8a,b). To estimate ARFs in V2
and V3, we used our own measures of mrf and summation field sizes
(Levitt et al., 1994; Gegenfurtner et al., 1997; this study). MT RF
sizes were taken from studies by Albright and Desimone (1987) and
Maunsell and Van Essen (1987). Estimated sizes of D° and
ARF were consistent with those determined physiologically (see Fig.
8a).
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RESULTS |
In a first set of single-unit recording experiments, we determined
quantitatively the spatial dimension of the RF and modulatory surround
field of V1 cells. In a second set of combined anatomical and
physiological experiments, we determined the visuotopic extent of V1
horizontal connections and of feedback connections from extrastriate
cortex to V1 and compared them with V1 cells' receptive field and
surround field sizes measured in the previous set of experiments. The
two sets of experiments were performed in different animals but in the
same region of visual space (2-8° retinal eccentricity in the lower
visual field representation of V1).
Spatial extent of V1 neuron receptive field and modulatory
surround field
Area summation curves were measured for 59 neurons sampled from
all layers of macaque V1 (n = 18 in layers 2/3;
n = 24 in layer 4; and n = 17 in layers
5/6) between 2 and 8° eccentricity. Of these cells, 69% had complex
RFs; the rest were simple cells (for a detailed report of these data,
see Levitt and Lund, 2002). A high-contrast (75%) drifting grating
patch of optimal stimulus parameters for the recorded neuron was
centered over the computer-mapped RF of the cell, and its diameter was
systematically increased. We measured response amplitude as a function
of stimulus diameter. Typically, responses increased with patch size to
a peak and either asymptoted at the peak or showed response suppression
as stimulus size was further increased (i.e., surround suppression)
(Fig. 2a). We took as a
measure of RF size the smallest stimulus diameter at peak response
(Fig. 2a; we included in this analysis only cells that
showed surround suppression). We refer to this measure of RF size as
the high-contrast SF. SFs for our sample of V1 cells averaged 1.0 ± 0.1° (Fig. 2b), increased with retinal eccentricity (Fig. 2c, middle function), and showed no
statistically significant variation across cortical layers despite a
trend for the largest SFs to be found in deeper layers. These results
on layer differences in SF sizes are consistent with those from other
studies (Sceniak et al., 2001; Cavanaugh et al., 2002; Levitt and Lund,
2002). RF size has been shown to vary depending on the method and the stimulus contrast used to measure it. Figure 2c compares RF
size as a function of eccentricity using three different test
conditions. Figure 2c, middle function, shows our
measure of high-contrast SF size as a function of retinal eccentricity.
Figure 2c, bottom function, shows data from Dow
et al. (1981), who measured RF size by moving a high-contrast bar of
light and hand drawing the contours of the area of visual space that
elicited spikes from the neuron. This measure of RF size is commonly
known as mrf or "classical" RF (Barlow et al., 1967). Our mean
high-contrast SFs were 2.2-fold greater than the mean mrf sizes of Dow
et al. (1981). Furthermore, RF size depends on stimulus contrast
(Kapadia et al., 1999; Sceniak et al., 1999). Sceniak et al. (1999)
found that, for the same V1 cells, SFs were on average 2.3-fold greater
when measured using low-contrast rather than high-contrast gratings
(Fig. 2c, top function).
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Figure 2.
Extent of RF and surround field for a population
of macaque V1 cells. a, Response of a representative V1
neuron to an optimal high-contrast grating patch of increasing diameter
(top right symbol). Patch diameter at peak
response (left arrow) was taken to be the size of the SF
of the cell in b and c (middle function).
Patch diameter at asymptotic response (right arrow) was
taken to be the size of the surround field of the cell in
d and e. b, Distribution
of SF diameters for a population of V1 neurons (n = 59), measured as in a. Arrowhead, Mean.
c, RF size as a function of retinal eccentricity
measured under three different test conditions, each one indicated by
symbols to the right of each
line. Straight lines are regression lines. Middle
function, SFs measured using expanding high-contrast (75%)
gratings; data from this study (n = 59 cells).
Bottom function, Hand-mapped mrf; based on data from Dow
et al. (1981). Top function, SFs measured using
expanding low-contrast gratings; based on data from Sceniak et al.
(1999) and obtained by multiplying our high-contrast SF function
(middle function) by 2.3. Stars, Means.
d-f, Distributions of surround field diameters for a
population of V1 cells measured under three different test conditions,
each one indicated by top right symbols.
d, Expanding high-contrast optimal grating stimulus,
including only cells with suppressive surrounds (n = 59, same cells as in b; note different scale on
x-axis in b and d).
e, Optimal center grating stimulus surrounded by
expanding most suppressive grating stimulus (n = 30, subset of cells in b and d).
f, Optimal center grating and most suppressive surround
grating stimuli plus blank annulus expanding in the surround
(n = 30 cells, same cells as in e).
Arrowheads in d-f, Means.
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For the same V1 cells, we also measured the extent of the modulatory
surround field using three different methods (Fig.
2d-f). Figure 2d shows the distribution
of surround sizes measured for 59 neurons using expanding high-contrast
gratings. As stimulus size increased beyond the high-contrast SF of the
cells, responses decreased. Surround size was defined as the smallest
stimulus diameter at which the response of the neuron asymptoted (Fig. 2a). Surround sizes ranged between 1.2 and >13° (13°
was the largest stimulus diameter we could produce on our monitor),
averaging 5.1 ± 0.6°. For a subset (n = 30) of
these cells, surround sizes were measured using two additional methods.
A center optimal grating stimulus was confined to a central region the
size of the high-contrast SF of the cell and was surrounded by the most
suppressive grating stimulus configuration (usually, but not always, a
grating at the same orientation as in the center). We then
systematically varied either the outer diameter of the surround
stimulus from 0° (i.e., central stimulus alone) to 13° (diameter of
the display screen) (Fig. 2e) or of a blank annulus
introduced between the central stimulus and a full-field (13°)
surround stimulus (Fig. 2f). Because the strength of
surround suppression has been shown to be highest in the region
abutting the RF center (Walker et al., 1999), by blanking out the
region of maximal surround strength (as in Fig. 2f),
we aimed at revealing the most remote surround influences. As surround
outer diameter increased, responses decreased; as annulus outer
diameter increased, responses increased. Surround and annulus outer
diameters at which responses asymptoted were taken as measures of
surround sizes (Fig. 2a,f, respectively). Under all test
conditions, surround diameters were found to extend up to and >13°.
However, different distributions and mean values [mean, 5.0 ± 0.6° (Fig. 2e) and 7.1 ± 0.2° (Fig.
2f)] were obtained with the different test methods,
reflecting the fact that the surround region is most suppressive close
to the RF. Thus, masking out the most suppressive near surround, as in
Figure 2f, revealed more distant influences, whereas the
latter were masked by optimally stimulating the most suppressive
near-surround region, as in Figure 2e. Surround sizes did
not vary significantly with retinal eccentricity or cortical layer. For
each neuron, we calculated a "relative" surround extent as the
ratio of surround field diameter (measured as in Fig. 2d) to
the high-contrast SF diameter; the population average was 4.6 ± 0.7.
To summarize, in V1 at 2-8° eccentricity, surround field sizes were
on average 4.6 (up to >13) times larger than high-contrast SF sizes
and at least 10 (up to >27) times larger than the mean mrf size of V1 cells.
Several other recent studies have examined the spatial summation
properties of macaque V1 neurons (Sceniak et al., 2001; Cavanaugh et
al., 2002). In these studies, center and surround responses were
modeled as independent, spatially overlapped excitatory and inhibitory
mechanisms, each with a Gaussian spatial sensitivity profile and with
the inhibitory mechanism being broader than the excitatory one (also
see DeAngelis et al., 1994). Cavanaugh et al. (2002) found that a ratio
of Gaussian model was the best fit to their data, whereas Sceniak
et al. (2001) favored a difference of Gaussian (DOG) model. The spatial
spread of the center and surround mechanisms in these studies was
estimated directly, and in one study (Sceniak et al., 2001)
exclusively, from the fitted curves. In the present study, we fit our
spatial summation data to a DOG model and used the fits mainly to
derive robust estimates of SF and surround field sizes. Because the
parameters derived from the Gaussian sensitivity functions depend
strongly on assumptions about the mechanisms underlying center-surround
interactions that may not be valid, we chose to report empirical
measurements of SF and surround sizes. However, because the DOG model
is a good descriptor of our summation data, and to allow for comparison with previous studies, we also derived from the fitted curves the
Gaussian spread (radius) of the excitatory and inhibitory components
(Sceniak et al., 2001) (for details, see Levitt and Lund, 2002). The
population means were 1.2° for the excitatory radius and 2.7° for
the inhibitory radius, revealing a somewhat larger mean RF center
mechanism than our empirical measurements of high-contrast SF size. The
width of the surround inhibitory mechanism instead agreed well with our
empirical measurements of surround size as described in Figure 2,
d and e. These results are consistent with data
from Sceniak et al. (2001), although our model parameters are somewhat
larger than those reported by Cavanaugh et al. (2002).
Cortical extent and patterns of horizontal and
feedback connections
CTB (n = 8) or BDA (n = 2)
injections (uptake zone diameters, 0.27-1.2 mm) were made in
physiologically characterized V1 loci at different cortical depths
(n = 2 in layers 1-3, 5 in layers 1-4C, 1 in layers
1-5, and 2 in layers 1-6) between 2.5 and 7.5° eccentricity in the
lower visual field representation. Consistent with previous results
obtained with different anatomical tracers (Rockland and Lund, 1983;
Yoshioka et al., 1996), CTB or BDA injections in macaque V1 layers 2/3
produced patches of terminal label surrounding the injected V1 column
(Fig. 3). CTB additionally retrogradely labeled cell bodies (but not fibers) within each patch, indicating the
reciprocal nature of these connections (Fig. 3, inset).
Reciprocal lateral connections were also labeled in layers 4B/upper
4C and 5/6, when the tracer injection involved these V1 laminas.
Both tracers revealed different patterns of label in these layers: bar-shaped fields in 4B/upper 4C (Asi et al., 1996; Angelucci et
al., 2002) and a less patchy, more diffuse label in 5/6 (Rockland and
Knutson, 2001). The labeled fields of lateral connections in all V1
layers were anisotropic in cortical space (Fig. 3). In layers 2/3, the
longer axis of label (D(mm)) (Fig.
1b), known to extend orthogonal to the ocular dominance
domains (Yoshioka et al., 1996), measured on average 6 ± 0.7 mm
(extending up to 9 mm). The distance from the edge of the tracer uptake
zone to the farthest labeled cell averaged 2.9 ± 0.4 mm. The most
distant labeled cells were consistently located laterally to the
injection site, i.e., toward the foveal representation of V1 (Fig. 3).
Furthermore, the mean anisotropy ratio (extent of long/short axis) of
CTB-labeled layer 2/3 lateral connection fields was 1.56 ± 0.1, closely matching the anisotropy ratio (1.6) of the V1 magnification
factor in these layers due to the ocular dominance domains (Blasdel and
Campbell, 2001). The latter two observations suggest that lateral
connections follow the overall anisotropy of visual field
representation in V1. CTB and BDA injections produced similar results.
We found no statistically significant difference in the extent or
anisotropy ratio between lateral connections in different V1 layers,
despite a trend for connections to be more extensive and more
anisotropic in the deeper layers. The extent and anisotropy ratio for
lateral connections in different V1 laminas are reported in Table
1, top.
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Figure 3.
Patchy lateral (or horizontal) connections in
layers 2/3 of macaque area V1. A surface view 2D composite
reconstruction of CTB-labeled connections is shown. The labeled field
axes measured 9 × 6 mm. Black oval, CTB uptake
zone; blank annulus, region of heavy label. Note
anisotropic distribution of overall label. The foveal representation is
toward the bottom (lateral V1); the V1-V2 border is to
the right (anterior V1). Small square,
Labeled patch shown at higher power in the inset. Scale
bar, 500 µm (corrected for 30% shrinkage). Inset,
High-power drawing of patch in the small square, showing
labeled fibers and somata (dots), indicating reciprocity
of connections. Scale bar, 100 µm.
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The same V1 injections (n = 10) used to determine the
extent of intra-areal V1 lateral connections labeled retrogradely the cells of origin of FB connections to V1 in extrastriate cortex (Fig.
4a). We confined our analysis
to FB from areas V2, V3, and MT. Small (~300-µm-diameter) tracer
injections confined to V1 layers 1-3 retrogradely labeled extensive
fields of somata in the superficial (2/3A) and deeper (at the 5/6
border) layers of area V2; injections involving layers 1-4B or 1-6
additionally labeled cells in the upper and lower layers of areas V3
and MT. Within each extrastriate area, the retrograde label in the
upper layers was less dense (Barone et al., 2000) and significantly (p < 0.01) less extensive than in layers 5/6
(Fig. 4b), and decreased in density and spatial extent with
distance from V1, whereas the label in the lower layers increased in
spatial extent (Table 1, middle). The density of labeled cells within
the FB fields gradually declined with distance from a denser center
core region. The retrograde label appeared clustered in the upper
layers and showed fluctuations in cell density in the lower layers.
Labeled FB fields in extrastriate cortex were anisotropic in cortical
space (Fig. 4b; Table 1, middle), their long axis following
the overall anisotropy of visual field representation of
the cortical area. Thus, in V2, the longer axis of the label extended
orthogonal to the CO bands, and in all areas was approximately parallel
to the longer (i.e., elevation) axis of the cortical area itself.
Extent and anisotropy ratios for retrogradely labeled FB connections in
the upper and lower layers of extrastriate cortex are reported in Table
1, middle.
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Figure 4.
Cells of origin in area V3 of feedback connections
to V1. a, Micrograph (left) of a sagittal
section through dorsal V3 (shaded box on the
right shows location of the photographed region on the
annectant gyrus), showing CTB-labeled cell bodies
(arrows) in layers 2/3A and 5/6. Cortical layers are
indicated at the bottom; WM, White
matter; arrowhead, labeled fibers in layers 4 and 3B
(terminals of feedforward connections from V1). The composite surface
map for this case is shown in b. The injection site
involved V1 layers 1-4C and was made at 6.5° eccentricity in the
lower visual field (same injection case as in Figs. 6a,
7a). D, Dorsal; P,
posterior. Scale bar, 100 µm. b, Surface view plots of
cell label density in the upper (left) and lower
(right) layers of dorsal V3, generated using custom
software written in Matlab. Color scale represents cell
density (numbers are cells per 500 µm2). Bins
containing <5% of peak cell density were removed from the image.
Label anterior to the crown of the annectant gyrus
(purple triangles in a,
b) is in area V3A. Purple squares (in
a, b), Location of the fundus of the lunate sulcus. The
long axis of these feedback fields measured 7.8 mm in the upper layers
and 9.8 mm in the lower layers. The visual field map of the lower-layer
feedback field is shown in Figure 7a. M,
Medial (away from the fovea); P, posterior (toward the
V1-V2 border). Scale bar, 1 mm (corrected for 30 and 12% shrinkage in
the anteroposterior and mediolateral axis, respectively).
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Our V1 injections were either confined to the CO interblob columns
(n = 2 injections through layers 1-3, and
n = 1 injection through layers 1-4B) or involved both
CO blob and interblob compartments (n = 7). Resulting
retrograde FB label involved all V2 stripe compartments, even in cases
in which the V1 injection was clearly confined to an interblob column.
The anterograde label in V2 (terminals of feedforward axons from V1)
arising from these same V1 injections in the interblob columns
(n = 3) was more focused than the retrograde (FB) label
and was either confined to the pale CO stripes (n = 1;
V1 injection in layers 1-3) or involved both the thick and pale
stripes (n = 2). There was no obvious difference in
extent between FB fields in extrastriate cortex labeled by V1
injections involving CO blob or interblob columns.
We also determined the extent of the divergence region of FB
connections to V1. This is the V1 region containing terminals of FB
axons, anterogradely labeled by small tracer injections in extrastriate
cortex. CTB or BDA injections (uptake zone diameter, 300-1500 µm)
were made in physiologically characterized loci in areas V2
(n = 2 CTB and 1 BDA injections) or dorsal V3
(n = 4 CTB injections) (Fig.
5a) between 2.2 and 6.5°
eccentricity in the lower visual field. To investigate the retinotopic
organization of FB connections to V1, all the V2 injected cases
(n = 3) received a second injection of a different
tracer (BDA or CTB) in V1 at the same retinal eccentricity as the V2
injection. Upper-layer injections in V2 or V3 produced large fields of
patchy terminal and cell body label in V1 layers 2/3 and 4B (Fig.
5b). Injections involving all V2 or V3 cortical laminas
resulted in even larger labeled fields within V1 and additionally
produced terminal and sparse cell body label at the layer 5/6 border of
V1. The layer 5/6 label appeared less clearly patchy than in the layers
above. Labeled patches in different V1 layers arising from the same
extrastriate injection were vertically aligned. Anterograde and
retrograde labels overlapped in the V1 patches, indicating the
reciprocal nature of feedforward and feedback connections to and
from V1. FB fields within V1 arising from tracer injections
in V2 or V3 greatly exceeded the size of the intra-areal V1 fields
produced by similarly sized V1 injections, the V3 injections labeling
larger fields in V1 than the V2 injections (Table 1, bottom). The FB fields in V1 were anisotropic in cortical space (Fig. 5c),
their longer axis extending parallel to the V1-V2 border when near
that border; their mean anisotropy ratio was greater than that of V1 intra-areal lateral connections (Table 1,bottom).
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Figure 5.
Patchy terminal label of feedback connections in
layer 4B of V1 arising from a tracer injection in area V3.
a, Micrograph of a sagittal section through dorsal area
V3, showing a CTB injection site involving all cortical layers (layer 1 is involved in the injection but not in this specific section). The
injection was made at 6.4° eccentricity in the lower visual field.
1, Layer 1; WM, white matter;
AG, annectant gyrus. Scale bar, 200 µm (corrected for
30% shrinkage). b, Micrograph showing a surface view of
CTB-labeled terminals and cell bodies (arising from the injection site
in a) in a single tissue section cut tangentially
through V1 layer 4B. c, 2D composite serial tangential
section reconstruction of anterograde (i.e., feedback) terminal label
through the whole thickness of layer 4B. Arrowheads in
b and c point to the same two patches.
Note anisotropic distribution of overall label. The axes of the labeled
field measured 13.8 × 8.1 mm. The visual field extent of this
layer 4B-labeled field is represented as a gray oval in
Figure 8b. Scale bar, 1 mm, for b and
c (corrected for 30% shrinkage). Medial,
Away from the fovea; Anterior: toward the V1-V2
border.
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Our V2 injections (one confined to a pale CO stripe and two involving
both thick and pale stripes) produced terminal and cell body labels in
the interblob columns of V1 (consistent with results of Sincich and
Horton, 2002). Terminal (FB) label in V1 arising from V3 injections was
confined either to the CO blob or to the interblob columns; larger
injections (~1.5 mm in diameter) labeled both V1 compartments.
These observations suggest that, similarly to corticocortical
projections between V1 and V2 (Sincich and Horton, 2002), the
connections between V1 and V3 form two parallel, segregated pathways,
one related to the CO blob columns of V1 and the other one related to
the interblobs (Angelucci and Levitt, 2002). We observed no obvious
difference in extent between FB fields terminating in different CO
compartments of V1.
Visuotopic extent of horizontal and feedback connections
Cortical measurements of intrinsic V1 and inter-areal FB fields
were converted into visual field coordinates and related to the spatial
extent of the receptive and surround fields of V1 cells.
Here we use two visuotopic measures: (1) D° is the extent,
in degrees of visual angle, of the axis of the connectional field, derived from the cortical retinotopic map (see Eqs. 1, 3) (Fig. 1a); its extent is independent of RF size; and (2) ARF is
the cumulative RF size of all labeled neurons in a given labeled
region; thus its extent is dependent on the method and stimulus
contrast used to measure RF size (see Eq. 4) (Fig. 1a). The
visuotopic extent (D°) of lateral connections is shown for
a representative case in Figure
6a. D° of
CTB-labeled layer 2/3 lateral connections (dashed gray
oval) is shown centered onto three different estimates of
the ARF size of the V1 injection (the three black ovals
indicate aggregate mrf and aggregate high- and low-contrast SF,
respectively). D° of V1 lateral connections in this case
was 2.2-fold greater than the aggregate mrf of the connections cells of
origin and closely matched the aggregate low-contrast SF size of the
cells of origin. Across the population, the monosynaptic spread
(D°) of V1 horizontal connections averaged 2.47 ± 0.3° in extent. V1 injection sites ranged in size between 0.2° and
0.8° (D°) or 0.5° and 1.3° (aggregate mrf). Because
our interest lay in determining whether lateral connections extend
beyond the limits of V1 cells RFs, we calculated a "relative"
visuotopic extent for these connections as the ratio of the visuotopic
extent of the connectional field (either D° or ARF size)
to the ARF size of its cells of origin. Figure 6b shows
population means of the relative visuotopic extent of V1 connectional
fields across all cortical layers (n = 21 connectional fields). Mean population values for the different V1 layers are shown
in Table 2. Ratios in Figure
6b and Table 2 are additionally shown for each of three
different methods of measuring RF size (mrf and high- and low-contrast
SF). On average, across the population, the monosynaptic spread
(D°) of V1 lateral connections was approximately three
times larger than the mrf and approximately two times larger than the
high-contrast SF of their cells of origin but was commensurate with the
low-contrast SF of the cells. Therefore, these connections could
account monosynaptically for the apparent expansion of the SF at low
contrast (Kapadia et al., 1999; Sceniak et al., 1999). However, because
V1 neuron surround fields were on average approximately five (up to
>13) times larger than the high-contrast SF of the neurons (see
above), V1 horizontal connections are significantly less extensive than
the mean surround size of V1 cells. Comparison of the mean visuotopic
extent of these connections (2.47°) with the mean Gaussian spread
(diameter) of the excitatory center (2.4°) and inhibitory surround
(5.4°) mechanisms also revealed that the monosynaptic spread of
horizontal connections is too small to account for mean surround size
and is instead commensurate with the size of the RF center
mechanism.
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Figure 6.
Visuotopic extent of V1 lateral connections.
a, Visual field map of a representative CTB injection
site and resulting labeled lateral connections in V1 layers 2/3. The
injection site was in the lower visual field representation of V1 at
6.5° eccentricity, 4° from the vertical meridian
(VM). HM, Horizontal meridian.
D° of the V1 connectional field (dashed gray
oval, 3 × 3.5°) and ARF size of the V1 injection site
(black ovals) were estimated as detailed in Materials
and Methods. The black ovals represent ARF sizes
computed using three different measures of RF size, each indicated by
symbols as in Figure 2c (aggregate mrf,
1.3 × 1.6°; aggregate high-contrast SF, 1.9 × 2.2°;
aggregate low-contrast SF, 3.4 × 3.7°). b,
Histogram of the population means (n = 21) of the
relative visuotopic extent of labeled V1 lateral connections along the
isopolar (black bars) and isoeccentricity
(hatched bars) axes of the labeled fields. Data from all
layers are pooled together. The visuotopic extent is expressed as the
ratio of D° of V1 connections to the ARF size of
neurons at the V1 injection site and is shown for each of three
different methods of measuring RF (and thus ARF) size
(symbols on x-axis, as in Fig.
2c). The trend for ratios to be smaller along the
isoeccentricity axis of the field was not statistically significant.
Error bars indicate SEM. The dashed horizontal line
marks a ratio of 1.
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Despite being anisotropic in cortical space (Fig. 3; Table 1, top), V1
lateral connections covered isotropic regions of visual space (Fig.
6a; Table 2). The ratio of D° of the foveal
half of the connections to D° of their peripheral half
averaged 0.94 ± 0.5, indicating that visual space is represented
symmetrically along the elevation axis of the connections. In addition,
the mean anisotropy ratio of their visual field extent (ARF size along the long axis/ARF size along the short axis of the labeled field) approached 1. There was no statistically significant difference in
anisotropy ratio across cortical layers, despite a tendency for
connections to be more anisotropic in layers 5/6 (Table 2).
We then asked whether the dimensions of feedback connections from
extrastriate cortex to V1 are commensurate with the scale of V1 neuron
modulatory surround fields. Because the cells of origin of FB
connections in extrastriate cortex and of lateral connections in V1
were labeled by the same V1 tracer injections (n = 10),
we were able to directly compare the extent of the visual field region
that these two different connectional systems convey to the same V1
column. Figure 7a shows an
example of the visuotopic extent of retrogradely labeled fields of
cells of origin of FB connections in layers 5/6 of extrastriate cortex.
The visuotopic extent of V1 horizontal connections to the same
injection site is also shown for comparison. The aggregate mrf sizes of
the FB fields in V2, V3, and MT were 4.6-, 7.7-, and 21-fold larger, respectively, than the aggregate mrf size of neurons at the V1 injection sites. In comparison, the aggregate mrf sizes of V1 intra-areal lateral connections in layers 2/3 and 4B were only 2.7 and
3.7 times larger than the aggregate mrf size of the same V1 injection.
Across the population, aggregate mrf sizes of retrogradely labeled FB
fields in the lower layers of extrastriate cortex averaged 3.8 ± 0.6° (in V2), 6.7 ± 0.7° (in V3), and 26.6 ± 3° (in
MT); those of V1 horizontal connections across all layers instead
averaged 2.9 ± 0.4. Figure 7b shows population means
of the relative visuotopic extent of retrogradely labeled FB fields in
the lower layers of areas V2, V3, and MT and, for comparison, of V1
lateral connections. Relative visuotopic extent values are shown in
Table 3 for each of two different methods
of measuring RF size. These results indicate that the region of visual
space conveyed by FB connections from extrastriate cortex to V1 is
larger than that conveyed by horizontal connections to the same V1
column. Furthermore, such visual space region increases with cortical
distance from V1, relating to the magnification factor and RF size of
neurons in the extrastriate region giving rise to the FB projections.
This was the case for both upper and lower layer FB fields, but within
each extrastriate area, the lower layer fields were always more
extensive than the upper layer fields (Table 3).
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Figure 7.
Visuotopic extent of retrogradely labeled fields
of cells of origin of FB connections in extrastriate cortex.
a, Visual field map of FB fields of neurons in layers
5/6 of areas V2 (top left), V3 (middle
right), and MT (top right) labeled by a CTB
injection through V1 layers 1-4C at 6.5° eccentricity (same
injection case as in Fig. 6a). Visual field maps of V1
lateral connections in layers 2/3 (bottom left) and 4B
(bottom right) labeled by the same V1 injection are also
shown. Gray circles, D° of the
connectional fields. Black ovals, aggregate mrf size of
neurons at the V1 injection site (1.3 × 1.6° in layers 2/3;
1.1 × 1.2° in layer 4B). Dashed black circles,
mean mrf size of cells at the edge of labeled fields. The aggregate mrf
size of each connectional field is the sum of the diameter of the
gray circle plus the diameter of one dashed black
circle. This was estimated as described in Materials and
Methods and measured 3.5 × 4.1° (V1 layers 2/3 horizontal
connections), 4.1 × 4.8° (V1 layer 4B horizontal connections),
6.1° (V2 FB), 8.7° (V3 FB), and 23.6° (MT FB). The aggregate mrf
of retrogradely labeled neuronal FB fields in the upper layers of
extrastriate cortex (data not shown) measured 5.4° (V2), 7.6° (V3),
and 15.3° (MT). Scale bar, 2°. b, Histogram of the
population means of the relative visuotopic extent of labeled layer 5/6
FB fields (black bars) in areas V2
(n = 6), V3 (n = 5), and MT
(n = 2), arising from the same V1 tracer
injections. The visuotopic extent is expressed as the ratio of the
aggregate mrf size of the FB field along its long axis to the
aggregate mrf size of neurons at the V1 injection site. White
bar, Mean aggregate mrf ratio (3.3 ± 0.24) for V1 lateral
connections (n = 21). Note cut on the
y-axis scale.
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We then compared the scale of FB fields with the scale of
physiologically measured surround field sizes of V1 neurons.
Specifically, we compared the relative visuotopic extent of FB fields
(Table 3) with the relative extent of surround fields of V1 neurons (see above). On average, depending on the cortical area of origin, FB
connections from the lower layers of extrastriate cortex conveyed information to a V1 column from regions of visual space 5-25 (up to
29) times the aggregate mrf of the V1 column, and 6-27 (up to 32)
times the aggregate high-contrast SF of the V1 injection (Table 3).
Surround field sizes of V1 cells were on average 10 (up to >27) times
larger than the mrf of the cells and 5 (up to >13) times larger than
their high-contrast SF (see above). Thus, the spatial scale of FB
connections from extrastriate cortex to V1 is commensurate with the
full spatial range of empirically measured modulatory surround fields
of single V1 cells. Similarly, comparison of the mean visuotopic extent
of FB fields with the mean Gaussian spread (diameter) of the inhibitory
surround mechanism (5.4°) revealed the mean visuotopic extent of FB
from V3 (5.6° in layers 2/3 and 6.7° in layers 5/6) to be
commensurate with the mean size of the RF surround mechanism, and FB
from V2 (3.4° in layers 2/3 and 3.8° in layers 5/6) and MT (15.3°
and 26.6° in the upper and lower layers) with shorter- and
longer-range surround sizes, respectively.
Figure 8, a and b,
shows the visuotopic extent of anterogradely labeled fields of
terminals of FB connections within V1 arising from a BDA injection in
V2 (Fig. 8a) or a CTB injection in V3 (Fig. 8b).
The relative visuotopic extent (D° of FB field/aggregate mrf of neurons at the injection site) of the FB terminal field in
layers 2/3 of V1 labeled by the V2 injection was 0.85 (Fig. 8a); those of the terminal FB fields in V1 layers 4B and 5/6
labeled by the V3 injection were 1.1 and 1, respectively. Across the
population, the visuotopic extent (D°) of FB terminal
fields in V1 labeled by V2 or V3 injections averaged 3.42 ± 1.2° (D° of the injection sites ranging between 0.3 and
2.7° and the aggregate mrf between 1.5 and 7.2°). Figure
8c and Table 4 show population
means of the relative visuotopic extent (D° or aggregate
mrf of FB field in V1/aggregate mrf of extrastriate injection site) of
anterogradely labeled FB fields across all layers of V1. These results
indicate that the aggregate mrf of FB terminal fields within V1 arising from V2 or V3 injections is commensurate with the aggregate mrf of FB
neurons at the injected site; i.e., FB connections link equal regions
of visual field in striate and extrastriate cortices. Injections in
overlapping retinotopic locations in V1 and V2 further emphasized the
orderly topographic organization of these connections, demonstrating
that FB neurons project symmetrically to V1 around a central point at
the same retinotopic location as the injected V2 column (Fig.
8a, bottom). Unlike V1 intra-areal lateral
connections, FB connectional fields in V1 were anisotropic in visual
space (Fig. 8a, top, b; Table 4).
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Figure 8.
Visuotopic extent of feedback terminal fields
anterogradely labeled in V1 by tracer injections in V2 or V3.
a, FB field in V1 arising from a V2 injection.
Bottom, Surface-view 2D serial tangential section
reconstruction of the FB terminal field in layers 2/3 of V1 labeled by
a BDA injection through V2 layers 1-6 at ~2° eccentricity in the
lower visual field. The arrow shows the approximate
location of the V1-V2 border [vertical meridian
(VM)] and points toward the fovea. Dots
1-9, V1 recording sites; numbers correspond to
RFs mapped at the top. Star, Center of
CTB V1 injection made at the same retinal eccentricity as the V2
injection. The labeled field axes measured 7.6 × 4 mm. Scale bar,
1 mm (corrected for 8% shrinkage). Top, Visual field
map of the BDA-labeled FB terminal field shown at the
bottom. Black oval, Estimated aggregate mrf of neurons at the V2 injection site
(1.6 × 1.15°); gray oval, estimated
D° of resulting labeled FB terminal field in V1
(1.35°x1°). Dashed rectangles, Three RFs (mrf) at V2
injection site recorded in the same vertical penetration at different
cortical depths (L3, L5, L6, V2 cortical layers 3, 5, 6, respectively). Gray rectangles, Four RFs (mrf) at V1
injection site (star at the bottom)
recorded in the same vertical penetration in different layers (most
superficial in layer 2, deepest in layer 6). Note good overlap of RFs
at V1 and V2 injected points, and their location at the center of the
FB terminal field. Rectangles 1-9, mrf sizes of neurons
at V1 recording sites 1-9 shown at the bottom.
Filled black rectangle, Foveal RF mapped to monitor eye
movements. Note good agreement between estimated and empirically
measured visuotopic extents of connections and injection sites.
b, Estimated visuotopic extent of labeled FB terminal
fields in V1 layers 4B (gray oval, 7.7 × 5.6°) and 5/6 (dashed gray oval, 7.1 × 5.3°)
arising from a CTB injection (black oval, 7.2 × 6.6°) through V3 layers 1-6 at 6.4° eccentricity in the lower
visual field. c, Histogram of the population means of
the relative visuotopic extent of labeled FB terminal fields in V1
(isopolar axis) arising from V2 or V3 injections. The visuotopic extent
is expressed as the ratio of D° of the FB fields to
the aggregate mrf size of neurons at the extrastriate injection site.
Data from all V1 layers are pooled together.
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DISCUSSION |
Our results show that the monosynaptic spread of horizontal
connections in macaque V1 is commensurate with the low-contrast summation field of V1 neurons. These connections are not sufficiently extensive to account for the mean size of V1 cells' surround fields or
longer-range center-surround interactions. Feedback connections from
extrastriate cortex to V1, instead, are commensurate with the full
range of V1 cells' center and surround field sizes; they show an
orderly topographic organization and terminate in a patch-like manner
within V1 (Fig. 9). These results
strongly suggest that V1 horizontal connections integrate signals
within the SF, whereas feedback connections underlie interactions
within and beyond the SF of V1 neurons.
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Figure 9.
Summary diagram showing the spatial scales of V1
lateral and feedback connections relative to the spatial scales of
empirically measured summation receptive field and modulatory surround
field of V1 neurons. Gray area, Region over which
presentation of stimuli at the same orientation as the center stimulus
can suppress the center response to an optimally oriented high contrast
stimulus. White area, Region over which presentation of
optimally oriented high-contrast stimuli evokes or facilitates a
response from the neuron (high-contrast SF). Hatched gray
annulus, Region over which presentation of stimuli at the same
orientation as the center stimulus can suppress or facilitate the
center response to an optimally oriented stimulus depending on the
center stimulus contrast. Lateral connections within V1
(red) extend beyond the high-contrast summation field
(black circle) and are commensurate with the
low-contrast SF (dashed black circle) of the V1 neurons
from which they arise. Feedback connections
(FB; blue) from extrastriate cortex to V1
are commensurate with the full spatial scale of the SF and surround
field. FB from "higher" cortical areas is more extensive than FB
from "lower" areas. Both connectional systems (lateral and FB) are
patchy in V1. Scale bar, 1°. We have previously proposed a model of
how FB and lateral connections might mediate modulation of RF responses
(Angelucci et al., 2002). In this model, the output of each excitatory
pyramidal neuron (e.g., the center recorded neuron) in V1 is controlled
by a local inhibitory neuron having higher response gain and contrast
threshold than the pyramid (Lund et al., 1995; Somers et al., 2002). FB
and lateral inputs contact directly both neuron types, whereas
feedforward inputs are only to the pyramid. The divergent-convergent
organization of FB and lateral axons is such that these two systems
overlap in space and are active for any stimulus diameter, even for
stimuli confined to the RF center. At low contrast, RF excitation
predominates; lateral and FB input to the pyramid can be summed from
more distant cortical (and visual space) locations before inhibition
begins to rise. Suppression of the center neuron response would result
from increasing the weight of excitation onto the pyramid and its local
inhibitory neuron, either via high-contrast feedforward drive or via
lateral and FB inputs, such as by increasing stimulus diameter.
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The size of the RF depends on the method used to measure it. The mrf is
the low-threshold, spiking region, which can be mapped using moving
small stimuli. This region is surrounded by a higher-threshold, depolarizing field, incapable of driving the cell when stimulated in
isolation but capable of increasing the response of the cell to
stimulation of its mrf (Bringuier et al., 1999). The size of this
subthreshold field surrounding the mrf has been measured intracellularly in cat V1 neurons and was found to be coextensive with
the monosynaptic spread of V1 horizontal connections in this species
(Bringuier et al., 1999). This larger subthreshold region can be
revealed extracellularly in areal summation experiments, using
expanding gratings, and has been shown to be larger when measured at
low stimulus contrast (Kapadia et al., 1999; Sceniak et al., 1999). In
the present study, we found the monosynaptic spread of horizontal
connections in monkey V1 to be coextensive with the empirically
measured low-contrast SF of V1 cells and with the mean Gaussian spread
of the excitatory center mechanism. Thus, the subthreshold depolarizing
synaptic integration field of V1 neurons, measured intracellularly by
Bringuier et al. (1999), most likely represents the low-contrast
summation field of the neurons measured extracellularly. In macaque,
feedforward thalamic afferents to single layer 4C V1 neurons are of
appropriate scale to underlie the mrf and, possibly, the high contrast
SF of these cells (Angelucci et al., 2002) but are not sufficiently
extensive to mediate longer-range interactions. Thus, we suggest that
intra-areal V1 horizontal connections play an important role in shaping
the spatial summation properties of V1 neurons at low contrast.
Somehow, the inputs from laterally offset neurons are more effective in driving the center neuron in a low-contrast regimen, when feedforward (lateral geniculate nucleus) inputs are only moderately driving the response of the center neuron (for a model, see Angelucci et al.,
2002) (Fig. 9).
We were surprised to find that horizontal connections in macaque V1 are
isotropic in visual space. This contrasts with results in other
species, in which these connections are anisotropic along an axis
colinear to the optimal orientation in the visual field map [tree
shrew (Bosking et al., 1997), cat (Schmidt et al., 1997), and
owl monkey (Sincich and Blasdel, 2001)]. Anisotropic
lateral connections in visual field have been suggested to serve as an anatomical substrate for intracortical generation of orientation selectivity or for contour completion in V1 (Bosking et al., 1997; Li,
1999; Sincich and Blasdel, 2001). The visual space anisotropy of V1
lateral connections seen in other species might, instead, reflect the
longer-length summation receptive fields of V1 cells, which have been
demonstrated at least in the tree shrew (Bosking and Fitzpatrick,
1995). Consistent with this hypothesis are the observations that
summation fields in macaque V1 are generally isotropic (Sceniak et al.,
2001; Levitt and Lund, 2002), and that both horizontal connections
(this study) and summation fields (Sceniak et al., 2001) are more
anisotropic in layer 6 than in more superficial layers of macaque V1.
Our results suggest that visual field anisotropy is not required to
generate orientation-selective RFs. Our finding that feedback terminal
fields in V1 show visual field anisotropy suggests that contour
completion in macaque V1 might instead be mediated by feedback connections.
The monosynaptic spread of horizontal connections is not sufficiently
extensive to account for the scale of the modulatory surround region
beyond the low-contrast SF of V1 neurons. However, the region between
the high- and low-contrast SF (Fig. 9, hatched annulus) can
suppress or facilitate the center response depending on the contrast of
the center stimulus (Levitt and Lund, 1997; Polat et al., 1998; Sceniak
et al., 1999, 2001; Mizobe et al., 2001) (for discussion, see Angelucci
and Bullier 2002). Thus, monosynaptic horizontal connections could
mediate surround modulation within this region of space. One example of
such "short-range" surround modulation is colinear facilitation,
i.e., enhancement of the mrf center response to an optimally oriented
low-contrast stimulus by flanking co-oriented and coaxial high-contrast
stimuli; a phenomenon thought to underlie perceptual grouping of
contour elements (Hess and Field, 2000). One interpretation of colinear facilitation is that it simply reflects placement of flank stimuli within the low-contrast SF of the same cell, and could thus be explained by the same mechanism underlying the expansion of the RF at
low contrast (for "long-range" colinear facilitation, see Mizobe et
al., 2001). Recent evidence that GABA inactivation of laterally
displaced V1 sites reduces colinear facilitation suggests that
horizontal connections may be the underlying anatomical substrate (Crook et al., 2002). Short-range surround suppression can also be
observed for high-contrast center stimuli. The same connectional system, and thus a similar inhibitory mechanism, could account for
"shrinkage" of the RF and short-range surround suppression at high
contrast (Angelucci et al., 2002) (Fig. 9) [see Sceniak et al. (1999)
for an alternative model]. Whether short-range surround suppression is
generated via lateral (Hupé et al., 2001b) or feedback
connections, it is clear that lateral connections are less extensive
than even the empirically measured mean SF size of V1 neurons or the
mean Gaussian spread of the inhibitory surround mechanism. Several
lines of evidence suggest that polysynaptic circuits of horizontal
connections within V1 are unlikely to underlie long-range
center-surround interactions. First, the strong inhibitory nature of
most surround effects would preclude propagation of signals through a
cascade of lateral connections. Because lateral axons are known to
target the same population of neurons at every synaptic location
(~80% excitatory and 20% inhibitory neurons; McGuire et al., 1991),
inhibition would occur at each relay step. Second, the slow conduction
velocity of horizontal axons (Bringuier et al., 1999; Girard et al.,
2001) would preclude them from processing fast information across long
distances, at least in V1 and V2 where, because of the large
magnification factor and small RF sizes, these connections connect
relatively small regions of space.
Inter-areal feedback projections provide information to a small column
of V1 neurons from larger regions of space than V1 lateral connections,
the size of the visual field region conveyed to V1 increasing with
cortical distance from V1. The visuotopic size of the feedback
projection field within V1 arising from a small column of extrastriate
cortical neurons matches the aggregate RF size of the extrastriate
neurons of origin, demonstrating an orderly topographic arrangement of
these connections. Our results show that feedback connections are of
appropriate scale to underlie long-range modulatory effects within and
beyond the low-contrast SF of V1 neurons (Fig. 9). The influence of
feedback connections on the RF center response of recipient neurons has
long been known. Specifically, inactivation of areas V2 and MT reduces
the response of neurons in lower-order areas to visual stimulation of
their RF center (Sandell and Schiller, 1982; Mignard and Malpeli,
1991; Hupé et al., 1998, 2001a), suggesting that at least part of
the FB input normally sums with FF inputs. A role for feedback
connections in mediating center-surround interactions is supported by
recent evidence that inactivation of area MT reduces the suppressive effect of surround motion stimulation in V3, V2, and V1 neurons (Hupé et al., 1998). Furthermore, feedback from MT has been shown to act on the early part of the response, suggesting that it may act on
V1 neurons at the same time as feedforward signals from the thalamus
(Hupé et al., 2001a). Feedback connections' conduction velocities are as rapid as those of feedforward connections and 10 times faster than those of horizontal connections (Girard et al.,
2001). Because of these spatial and temporal properties, feedback
connections are well suited to convey fast visual signals across
distant parts of space. Contrary to previous reports that feedback
connections are more diffuse and nonspecific than feedforward connections (Rockland and Virga, 1989; Shipp and Zeki, 1989), we show
here that feedback projections are parcellated into discrete patches in
V1 and overlap with patches of V1 feedforward projecting neurons. The
precise alignment of labeled feedback terminal clusters in V1 with
clusters of feedforward efferent cells (Salin et al., 1995; Johnson and
Burkhalter, 1997), is well suited to fast transfer of specific
functional information to and from V1, and it may also explain the
orientation specificity of interactions between surround and RF
stimulus configuration. The periodicity of feedback connections, much
like that of intra-areal connections, matches the periodic distribution
of specific functional properties in V1, such as orientation
preference. Similarly to V1 lateral connections (Malach et al., 1993),
feedback connections appear to link points of like-orientation
preference (Gilbert and Wiesel, 1989; Shmuel et al., 1998). Previously
we have proposed a detailed model of how feedback connections might
mediate orientation specific modulation of RF responses (Angelucci et
al., 2002) (Fig. 9). Although patchy feedback connections in V1 appear
to reflect linking of similar stimulus attributes in striate and
extrastriate cortex, the relationship of the feedback terminal patches
to the CO columns in V1 suggests also the existence of specific
compartments within V2 and V3, each compartment having a segregated
terminal territory in V1 (Angelucci and Levitt, 2002).
Although we are proposing that feedback connections may mediate
center-surround interactions in V1, a more general role for this
connectional system, consistent with their spatial scale, would be to
mediate global-to-local, top-down integration of visual information.
Global-to-local signal integration might represent an essential step in
visual processing and has been shown to occur in the responses of V1
and V2 cells to illusory contours (Lee and Nguyen, 2001) or to occluded
contours defined by contextual depth cues (Sugita, 1999; Bakin et al.,
2000).
| |
FOOTNOTES |
Received March 8, 2002; revised June 19, 2002; accepted June 27, 2002.
This work was supported by Medical Research Council Grants G9203679 and
G9408137, by European Community Grant Viprom Biomed 2, by Wellcome
Trust Grant 061113, in part by National Institutes of Health Grants
EY12781 and Research Centers in Minority Institutions G12RR-03060, and by a grant from Research to Prevent Blindness, Inc.
(New York, NY) to the Department of Ophthalmology, University of Utah.
We thank Drs. Paul Bressloff and Robert Shapley for useful discussions,
Dr. Paul Bressloff and Gina Cantone for help with data analysis, and
Kesi Sainsbury for expert technical assistance. Dr. Niall McLoughlin
participated in some of the experiments.
Correspondence should be addressed to Alessandra Angelucci, Department
of Ophthalmology and Visual Science, Moran Eye Center, University of
Utah, 50 North Medical Drive, Salt Lake City, UT 84132. E-mail:
alessandra.angelucci{at}hsc.utah.edu.
J.-M. Hupé's present address: Center for Neural Science, New
York University, 4 Washington Place, New York, NY 10003.
| |
REFERENCES |
-
Albright TD,
Desimone R
(1987)
Local precision of visuotopic organization in the middle temporal area (MT) of the macaque.
Exp Brain Res
65:582-592[Web of Science][Medline].
-
Allman J,
Miezin F,
Mc Guinness E
(1985)
Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons.
Annu Rev Neurosci
8:407-430[Web of Science][Medline].
-
Angelucci A, Bullier J (2002) Reaching beyond the classical
receptive field of V1 neurons: horizontal or feedback axons? J
Physiol (Paris), in press.
-
Angelucci A, Levitt JB (2002) Convergence of color, motion
and form pathways in macaque V3. Soc Neurosci Abstr, in
press.
-
Angelucci A,
Clasca F,
Sur M
(1996)
Anterograde axonal tracing with the subunit B of cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains.
J Neurosci Methods
65:101-112[Web of Science][Medline].
-
Angelucci A,
Lund JS,
Walton E,
Levitt JB
(1998)
Retinotopy of connections within and between areas V1 to V5 of macaque visual cortex.
Soc Neurosci Abstr
24:897.
-
Angelucci A,
Levitt JB,
Hupé J-M,
Walton EJS,
Bullier J,
Lund JS
(2000)
Anatomical circuits for local and global integration of visual information: intrinsic and feedback connections in macaque visual cortical area V1.
Eur J Neurosci
12 [Suppl 11]:285[Medline].
-
Angelucci A,
Levitt JB,
Lund JS
(2002)
Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1.
Prog Brain Res
136:373-388[Medline].
-
Asi H,
Levitt JB,
Lund JS
(1996)
In macaque V1 lateral connections in layer 4B have a different topography than in layers 2/3.
Soc Neurosci Abstr
22:1608.
-
Bakin JS,
Nakayama K,
Gilbert CD
(2000)
Visual responses of monkey areas V1 and V2 to three-dimensional surface configurations.
J Neurosci
20:8188-8198[Abstract/Free Full Text].
-
Barlow HB,
Blakemore C,
Pettigrew JD
(1967)
The neural mechanisms of binocular depth discrimination.
J Physiol (Lond)
193:327-342[Abstract/Free Full Text].
-
Barone P,
Batardiere A,
Knoblauch K,
Kennedy H
(2000)
Laminar distribution of neurons in extrastriate areas projecting to visual areas V1 and V4 correlates with the hierarchical rank and indicates the operation of a distance rule.
J Neurosci
20:3263-3281[Abstract/Free Full Text].
-
Blakemore C,
Tobin EA
(1972)
Lateral inhibition between orientation detectors in the cat's visual cortex.
Exp Brain Res
15:439-440[Web of Science][Medline].
-
Blasdel GG,
Campbell D
(2001)
Functional retinotopy of monkey visual cortex.
J Neurosci
21:8286-8301[Abstract/Free Full Text].
-
Bosking WH,
Fitzpatrick D
(1995)
Physiological correlates of anisotropy in horizontal connections: length summation properties of neurons in layers 2 and 3 of tree shrew striate cortex.
Soc Neurosci Abstr
21:1751.
-
Bosking WH,
Zhang Y,
Schofield B,
Fitzpatrick D
(1997)
Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex.
J Neurosci
17:2112-2127[Abstract/Free Full Text].
-
Bringuier V,
Chavane F,
Glaeser L,
Frégnac Y
(1999)
Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons.
Science
283:695-699[Abstract/Free Full Text].
-
Burkhalter A,
Felleman DJ,
Newsome WT,
Van Essen DC
(1986)
Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex.
Vision Res
26:63-80[Web of Science][Medline].
-
Cavanaugh JR, Bair W, Movshon JA (2002) Nature and
interaction of signals from the receptive field center and surround in
macaque V1 neurons. J Neurophysiol, in press.
-
Crick F,
Koch C
(1998)
Constraints on cortical and thalamic projections: the no-strong-loops hypothesis.
Nature
391:245-250[Medline].
-
Crook JM,
Engelmann R,
Löwell S
(2002)
GABA-inactivation attenuates colinear facilitation in cat primary visual cortex.
Exp Brain Res
143:295-302[Web of Science][Medline].
-
Das A,
Gilbert CD
(1995)
Receptive field expansion in adult visual cortex is linked to dynamic changes in strength of cortical connections.
J Neurophysiol
74:779-792[Abstract/Free Full Text].
-
DeAngelis GC,
Freeman RD,
Ohzawa I
(1994)
Length and width tuning of neurons in the cat's primary visual cortex.
J Neurophysiol
71:347-374[Abstract/Free Full Text].
-
Dow BM,
Snyder AZ,
Vautin RG,
Bauer R
(1981)
Magnification factor and receptive field size in foveal striate cortex of the monkey.
Exp Brain Res
44:213-228[Web of Science][Medline].
-
Dow BM,
Vautin RG,
Bauer R
(1985)
The mapping of visual space onto foveal striate cortex in the macaque monkey.
J Neurosci
5:890-902[Abstract].
-
Felleman DJ,
Van Essen DC
(1991)
Distributed hierarchical processing in the primate cerebral cortex.
Cereb Cortex
1:1-47[Abstract/Free Full Text].
-
Gallyas F
(1979)
Silver staining of myelin by means of physical development.
Neurol Res
1:203-209[Medline].
-
Gattas R,
Gross CG,
Sandell JH
(1981)
Visual topography of V2 in the macaque.
J Comp Neurol
201:519-539[Web of Science][Medline].
-
Gattas R,
Sousa APB,
Gross CG
(1988)
Visuotopic organization and extent of V3 and V4 of the macaque.
J Neurosci
8:1831-1845[Abstract].
-
Gegenfurtner KR,
Kiper DC,
Levitt JB
(1997)
Functional properties of neurons in macaque area V3.
J Neurophysiol
77:1906-1923[Abstract/Free Full Text].
-
Gilbert CD,
Wiesel TN
(1989)
columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex.
J Neurosci
9:2432-2442[Abstract].
-
Gilbert CD,
Wiesel TN
(1990)
The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat.
Vision Res
30:1689-1701[Web of Science][Medline].
-
Gilbert C,
Das A,
Ito M,
Kapadia M,
Westheimer G
(1996)
Spatial integration and cortical dynamics.
Proc Natl Acad Sci USA
93:615-622[Abstract/Free Full Text].
-
Girard P,
Hupé J-M,
Bullier J
(2001)
Feedforward and feedback connections between areas V1 and V2 of the monkey have similar rapid conduction velocities.
J Neurophysiol
85:1328-1331[Abstract/Free Full Text].
-
Hess R,
Field D
(2000)
Integration of contours: new insights.
Trends Cognit Sci
3:480-486.
-
Hupé J-M,
James AC,
Payne BR,
Lomber SG,
Girard P,
Bullier J
(1998)
Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons.
Nature
394:784-787[Medline].
-
Hupé J-M,
Chouvet G,
Bullier J
(1999)
Spatial and temporal parameters of cortical inactivation by GABA.
J Neurosci Methods
86:129-143[Web of Science][Medline].
-
Hupé J-M,
James AC,
Girard P,
Lomber SG,
Payne BR,
Bullier J
(2001a)
Feedback connections act on the early part of the responses in monkey visual cortex.
J Neurophysiol
85:134-145[Abstract/Free Full Text].
-
Hupé J-M,
James AC,
Girard P,
Bullier J
(2001b)
Response modulations by static texture surround in area V1 of the macaque monkey do not depend on feedback connections from V2.
J Neurophysiol
85:146-163[Abstract/Free Full Text].
-
Johnson PB,
Angelucci A,
Ziparo RM,
Minciacchi D,
Bentivoglio M,
Caminiti R
(1989)
Segregation and overlap of callosal and association neurons in frontal and parietal cortices of primates: a spectral and coherence analysis.
J Neurosci
9:2313-2326[Abstract].
-
Johnson RR,
Burkhalter A
(1997)
A polysynaptic feedback circuit in rat visual cortex.
J Neurosci
17:7129-7140[Abstract/Free Full Text].
-
Kapadia MK,
Ito M,
Gilbert CD,
Westheimer G
(1995)
Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys.
Neuron
15:843-856[Web of Science][Medline].
-
Kapadia MK,
Westheimer G,
Gilbert CD
(1999)
Dynamics of spatial summation in primary visual cortex of alert monkeys.
Proc Natl Acad Sci USA
96:12073-12078[Abstract/Free Full Text].
-
Knierim JJ,
Van Essen DC
(1992)
Neuronal responses to static texture patterns in area V1 of the alert macaque monkey.
J Neurophysiol
67:961-980[Abstract/Free Full Text].
-
Lanciego JL,
Luquin MR,
Guillén J,
Giménez-Amaya JM
(1998)
Multiple neuroanatomical tracing in primates.
Brain Res Protocols
2:323-332[Medline].
-
Lee TS,
Nguyen M
(2001)
Dynamics of subjective contour formation in the early visual cortex.
Proc Natl Acad Sci USA
98:1907-1911[Abstract/Free Full Text].
-
Levitt JB,
Lund JS
(1997)
Contrast dependence of contextual effects in primate visual cortex.
Nature
387:73-76[Medline].
-
Levitt JB, Lund JS (2002) The spatial extent over which
neurons in macaque striate cortex pool visual signals. Vis Neurosci, in
press.
-
Levitt JB,
Kiper DC,
Movshon JA
(1994)
Receptive fields and functional architecture of macaque V2.
J Neurophysiol
71:2517-2542[Abstract/Free Full Text].
-
Li Z
(1999)
Pre-attentive segmentation in the primary visual cortex.
Spatial Vision
13:25-50.
-
Lund JS,
Wu Q,
Hadingham PT,
Levitt JB
(1995)
Cells and circuits contributing to functional properties in area V1 of macaque monkey cerebral cortex: bases for neuroanatomically realistic models.
J Anat
187:563-581[Web of Science][Medline].
-
Malach R,
Amir Y,
Harel M,
Grinvald A
(1993)
Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex.
Proc Natl Acad Sci USA
90:10469-10473[Abstract/Free Full Text].
-
Maunsell JHR,
Van Essen DC
(1987)
Topographic organization of the middle temporal visual area in the macaque monkey: representational biases and the relationship to callosal connections and myeloarchitectonic boundaries.
J Comp Neurol
266:535-555[Web of Science][Medline].
-
McGuire BA,
Gilbert CD,
Rivlin PK,
Wiesel TN
(1991)
Targets of horizontal connections in macaque primary visual cortex.
J Comp Neurol
305:370-392[Web of Science][Medline].
-
Merril EG,
Ainsworth A
(1972)
Glass-coated platinum-plated tungsten microelectrodes.
Med Biol Eng
10:662-672[Web of Science][Medline].
-
Mignard M,
Malpeli JG
(1991)
Paths of information flow through visual cortex.
Science
251:1249-1251[Abstract/Free Full Text].
-
Mizobe K,
Polat U,
Pettet MW,
Kasamatsu T
(2001)
Facilitation and suppression of single striate-cell activity by spatially discrete pattern stimuli presented beyond the receptive field.
Vis Neurosci
18:377-391[Medline].
-
Nelson JI,
Frost B
(1978)
Orientation selective inhibition from beyond the classical receptive field.
Brain Res
139:359-365[Web of Science][Medline].
-
Nothdurft HC,
Gallant JL,
Van Essen DC
(1999)
Response modulation by texture surround in primate area V1: correlates of "popout" under anesthesia.
Vis Neurosci
16:15-34[Web of Science][Medline].
-
Perkel DJ,
Bullier J,
Kennedy H
(1986)
Topography of the afferent connectivity of area 17 in the macaque monkey: a double-labeling study.
J Comp Neurol
253:374-402[Web of Science][Medline].
-
Polat U,
Mizobe K,
Pettet MW,
Kasamatsu T,
Norcia AM
(1998)
Collinear stimuli regulate visual responses depending on cell's contrast threshold.
Nature
391:580-584[Medline].
-
Rockland KS,
Knutson T
(2001)
Axon collaterals of Meynert cells diverge over large portions of area V1 in the macaque monkey.
J Comp Neurol
441:134-147[Web of Science][Medline].
-
Rockland KS,
Lund JS
(1983)
Intrinsic laminar lattice connections in primate visual cortex.
J Comp Neurol
216:303-318[Web of Science][Medline].
-
Rockland KS,
Pandya DN
(1979)
Laminar origins and terminations of cortical connections to the occipital lobe in the rhesus monkey.
Brain Res
179:3-20[Web of Science][Medline].
-
Rockland KS,
Virga A
(1989)
Terminal arbors of individual "feedback" axons projecting from area V2 to V1 in the macaque monkey: a study using immunohistochemistry of anterogradely transported phaseolus vulgaris-leucoagglutinin.
J Comp Neurol
285:54-72[Web of Science][Medline].
-
Roe AW,
Ts'o DY
(1995)
Visual topography in primate V2: multiple representation across functional stripes.
J Neurosci
15:3689-3715[Abstract].
-
Salin PA,
Bullier J
(1995)
Corticocortical connections in the visual system: structure and function.
Physiol Rev
75:107-154[Free Full Text].
-
Salin PA,
Kennedy H,
Bullier J
(1995)
Spatial reciprocity of connections between areas 17 and 18 in the cat.
Can J Physiol Pharmacol
73:1339-1347[Web of Science][Medline].
-
Sandell JH,
Schiller PH
(1982)
Effect of cooling area 18 on striate cortex cells in the squirrel monkey.
J Neurophysiol
48:38-48[Free Full Text].
-
Sceniak MP,
Ringach DL,
Hawken MJ,
Shapley RM
(1999)
Contrast's effect on spatial summation by macaque V1 neurons.
Nat Neurosci
2:733-739[Web of Science][Medline].
-
Sceniak MP,
Hawken MJ,
Shapley RM
(2001)
Visual spatial characterization of macaque V1 neurons.
J Neurophysiol
85:1873-1887[Abstract/Free Full Text].
-
Schmidt KE,
Goebel R,
Löwell S,
Singer W
(1997)
The perceptual grouping criterion of colinearity is reflected by anisotropies of connections in the primary visual cortex.
Eur J Neurosci
9:1083-1089[Web of Science][Medline].
-
Shipp S,
Zeki S
(1989)
The organization of connections between areas V5 and V1 in macaque monkey visual cortex.
Eur J Neurosci
1:308-331.
-
Shmuel A,
Korman M,
Harel M,
Grinvald A,
Malach R
(1998)
Relationship of feedback connections from area V2 to orientation domains in area V1 of the primate.
Soc Neurosci Abstr
24:767.
-
Sincich LC,
Blasdel GG
(2001)
Oriented axon projections in primary visual cortex of the monkey.
J Neurosci
21:4416-4426[Abstract/Free Full Text].
-
Sincich LC,
Horton JC
(2002)
Divided by cytochrome oxidase: a map of the projections from V1 to V2 in macaques.
Science
295:1734-1737[Abstract/Free Full Text].
-
Somers D,
Dragoi V,
Sur M
(2002)
Orientation selectivity and its modulation by local and long-range connections in visual cortex.
In: The cat primary visual cortex (Payne BR,
Peters A,
eds), pp 471-520. San Diego: Academic.
-
Sugita Y
(1999)
Grouping of image fragments in primary visual cortex.
Nature
401:269-272[Medline].
-
Tootell RBH,
Switkes E,
Silverman MS,
Hamilton SL
(1988)
Functional anatomy of macaque striate cortex II: retinotopic organization.
J Neurosci
8:1531-1568[Abstract].
-
Van Essen DC,
Newsome WT,
Maunsell JH
(1984)
The visual field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability.
Vision Res
24:429-448[Web of Science][Medline].
-
Walker GA,
Ohzawa I,
Freeman RD
(1999)
Asymmetric suppression outside the classical receptive field of the visual cortex.
J Neurosci
19:10536-10553[Abstract/Free Full Text].
-
Yoshioka T,
Blasdel GG,
Levitt JB,
Lund JS
(1996)
Relation between patterns of intrinsic lateral connectivity, ocular dominance and cytochrome oxidase reactive regions in macaque monkey striate cortex.
Cereb Cortex
6:297-310[Abstract/Free Full Text].
Copyright © 2002 Society for Neuroscience 0270-6474/02/22198633-14$05.00/0
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|
|
|
|
|
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|
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|
|
|
|
|
|
|
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|
|
|
|
|
|
|
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[PDF]
|
|
|
|
|
|
|
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1789 - 1797.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Xing, R. M. Shapley, M. J. Hawken, and D. L. Ringach
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94(1):
799 - 812.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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9026 - 9031.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Chacron, L. Maler, and J. Bastian
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J. Neurosci.,
June 8, 2005;
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5521 - 5532.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C Horton and D. L Adams
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Phil Trans R Soc B,
April 29, 2005;
360(1456):
837 - 862.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Zhang, J. Zheng, I. Watanabe, I. Maruko, H. Bi, E. L. Smith III, and Y. Chino
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PNAS,
April 19, 2005;
102(16):
5862 - 5867.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Cai, A. V. Rangan, and D. W. McLaughlin
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PNAS,
April 19, 2005;
102(16):
5868 - 5873.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Shmuel, M. Korman, A. Sterkin, M. Harel, S. Ullman, R. Malach, and A. Grinvald
Retinotopic Axis Specificity and Selective Clustering of Feedback Projections from V2 to V1 in the Owl Monkey
J. Neurosci.,
February 23, 2005;
25(8):
2117 - 2131.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. G. Nowak, M. V. Sanchez-Vives, and D. A. McCormick
Role of Synaptic and Intrinsic Membrane Properties in Short-Term Receptive Field Dynamics in Cat Area 17
J. Neurosci.,
February 16, 2005;
25(7):
1866 - 1880.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. I. Baker, E. Peli, N. Knouf, and N. G. Kanwisher
Reorganization of Visual Processing in Macular Degeneration
J. Neurosci.,
January 19, 2005;
25(3):
614 - 618.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Ozeki, O. Sadakane, T. Akasaki, T. Naito, S. Shimegi, and H. Sato
Relationship between Excitation and Inhibition Underlying Size Tuning and Contextual Response Modulation in the Cat Primary Visual Cortex
J. Neurosci.,
February 11, 2004;
24(6):
1428 - 1438.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. G. Solomon, J. W. Peirce, and P. Lennie
The Impact of Suppressive Surrounds on Chromatic Properties of Cortical Neurons
J. Neurosci.,
January 7, 2004;
24(1):
148 - 160.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. A. McCormick, Y. Shu, A. Hasenstaub, M. Sanchez-Vives, M. Badoual, and T. Bal
Persistent Cortical Activity: Mechanisms of Generation and Effects on Neuronal Excitability
Cereb Cortex,
November 1, 2003;
13(11):
1219 - 1231.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. Bair, J. R. Cavanaugh, and J. A. Movshon
Time Course and Time-Distance Relationships for Surround Suppression in Macaque V1 Neurons
J. Neurosci.,
August 20, 2003;
23(20):
7690 - 7701.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Zenger-Landolt and D. J. Heeger
Response Suppression in V1 Agrees with Psychophysics of Surround Masking
J. Neurosci.,
July 30, 2003;
23(17):
6884 - 6893.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. J. Chisum, F. Mooser, and D. Fitzpatrick
Emergent Properties of Layer 2/3 Neurons Reflect the Collinear Arrangement of Horizontal Connections in Tree Shrew Visual Cortex
J. Neurosci.,
April 1, 2003;
23(7):
2947 - 2960.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. S. Lund, A. Angelucci, and P. C. Bressloff
Anatomical Substrates for Functional Columns in Macaque Monkey Primary Visual Cortex
Cereb Cortex,
January 1, 2003;
13(1):
15 - 24.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
TOP
ABSTRACT
INTRODUCTION
