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European Journal of Neuroscience, Vol. 16, pp. 945±956, 2002
ã Federation of European Neuroscience Societies
Convergence of parvocellular and magnocellular
information channels in the primary visual cortex of the
macaque
(corrected)
T. R. Vidyasagar1,2,3,², J. J. Kulikowski2,³, D. M. Lipnicki1 and B. Dreher1,2,§
1
School of Psychology,
2
John Curtin School of Medical Research and
3
Centre for Visual Science, Australian National University, Canberra, ACT 0200, Australia
This version is corrected
according to Erratum (last
paragraph of Results section)
Keywords: colour, dorsal lateral geniculate nucleus, luminance, parallel channels, primate, striate cortex
Abstract
We investigated whether responses of single cells in the striate cortex of anaesthetized macaque monkeys exhibit signatures of
both parvocellular (P) and magnocellular (M) inputs from the dorsal lateral geniculate nucleus (dLGN). We used a palette of 128
isoluminant hues at four different saturation levels to test responses to chromatic stimuli against a white background. Spectral
selectivity with these isoluminant stimuli was taken as an indication of P inputs. The presence of magnocellular inputs to a given
cortical cell was deduced from its responses to a battery of tests, including assessment of achromatic contrast sensitivity, relative
strengths of chromatic and luminance borders in driving the cell at different velocities and conduction velocity of their retinogeniculo-cortical afferents. At least a quarter of the cells in our cortical sample appear to receive convergent P and M inputs. We
cannot however, exclude the possibility that some of these cells could be receiving a convergent input from the third parallel
channel from the dLGN, namely the koniocellular (K) rather than the P channel. The neurons with convergent P and M inputs
were recorded not only from supragranular and infragranular layers but also from the principal geniculate input recipient layer 4.
Thus, our results challenge classical ideas of strict parallelism between different information streams at the level of the primate
striate cortex.
Introduction
In the primate retino-geniculate-cortical pathway, three distinct
parallel information channels have been described which carry
retinal information to the primary visual cortex (striate cortex,
cytoarchitectonic area 17 or area V1), namely the parvocellular (P),
the magnocellular (M) and koniocellular (K) channels (for reviews
see Livingstone & Hubel, 1988; Casagrande & Norton, 1991;
Goodale & Milner, 1992; Lachica et al., 1992; Casagrande & Kaas,
1994; Casagrande, 1994; DeYoe et al., 1994; Lund et al., 1994;
Callaway, 1998). The P, M and K pathways originate from
morphologically distinct classes of retinal ganglion cells and relay
in parallel through anatomically distinct layers in the dorsal lateral
geniculate nucleus (reviewed by Kaplan et al., 1990) to the primary
visual cortex. The P and M channels on which the great majority of
the studies to date have concentrated, are postulated to remain largely
segregated not only in the striate cortex (Bullier & Henry, 1980;
Livingstone & Hubel, 1988; Casagrande & Norton, 1991; Casagrande
Correspondence: Dr T. R. Vidyasagar, at ²present address below.
E-mail: trv@unimelb.edu.au
²
Present address: Department of Optometry and Vision Sciences, University
of Melbourne, Vic, 3053, Australia
³
Present address: Department of Optometry and Neuroscience, University of
Manchester Institute of Science and Technology, Manchester, UK
§
Present address: Department of Anatomy and Histology, Institute for
Biomedical Research (F13), University of Sydney, Sydney & NSW 2006,
Australia
Received 14 March 2002, revised 17 June 2002, accepted 18 June 2002
doi:10.1046/j.1460-9568.2002.02137.x
& Kaas, 1994) but also in their projections from the striate to the
extra-striate visual areas (Shipp & Zeki, 1985; Maunsell & Newsome,
1987; DeYoe & Van Essen, 1985, 1988; Livingstone & Hubel, 1988;
Zeki, 1993; DeYoe et al., 1994). Indeed, it has been suggested that
visual information processing proceeds from the striate cortex along
two major streams: one of them, the so-called dorsal stream, carries
largely the magnocellular information to the parietal cortex via a
number of extrastriate visual areas, while the other stream, the socalled ventral steam, again via a number of extrastriate visual areas,
carries largely the parvocellular information to the inferotemporal
cortex. However, recent anatomical and functional data indicate that
there might be a degree of convergence of these pathways in the
extrastriate areas (Maunsell et al., 1990; Ferrera et al., 1992, 1994;
Merigan & Maunsell, 1993; Gegenfurtner et al., 1996; Kiper et al.,
1997). Recent anatomical data also indicate that the ®rst level of
convergence between the parvocellular and magnocellular pathways
may occur as early as layer 4 of the striate cortex, the major input
layer for the geniculate afferents. The anatomical substrate for such
interaction is evident in the dendritic and axonal arborizations of
neurons in layers 4Ca and 4Cb (Lund et al., 1994; Levitt et al., 1994;
Yoshioka et al., 1994; Yabuta & Callaway, 1998). Furthermore: (i)
projection neurons in layer 3B of striate cortex, which until recently
were believed to send exclusively P type information to the ventral
stream, receive substantial direct excitatory input from layer 4Ca,
that is, from M pathway (Sawatari & Callaway, 2000); and (ii)
pyramidal neurons in layer 4B, which is generally believed to provide
an exclusive relay of M information channel to the dorsal stream,
946 T. R. Vidyasagar et al.
appear to receive (Yabuta et al., 2001) strong direct excitatory inputs
from both layers 4Ca (M pathway) and 4Cb (P pathway). In the
present study, we have examined the issue of functional convergence
of P and M information channels in the primary visual cortex by
recording the activity of single cells in the anaesthetized macaque's
striate cortex and examining their responses for the presence of
speci®c signatures of magnocellular and/or parvocellular inputs. In
the diurnal primates such as macaque monkeys, an important criterion
for revealing the presence of a parvocellular input to the cortical cell
is the presence of responses to chromatic, isoluminant contours and
spectral selectivity. There is a large body of evidence indicating that
in macaque monkeys magnocellular cells in the retina and the dLGN
are generally colour-blind (e.g. Wiesel & Hubel, 1966; Dreher et al.,
1976) and do not respond to isoluminant chromatic stimuli (Schiller
& Colby, 1983; Hubel & Livingstone, 1990; for review, see Kaplan
et al., 1990). Therefore, we took the presence of responses to
isoluminant stimuli and spectral selectivity of cortical neurons we
recorded from as clear indications of a P input. The converse is
however, not true, namely, the lack of response to isoluminant stimuli
does not necessarily indicate that the cell lacks P inputs.
To detect the presence of the suprathreshold magnocellular input to
a cortical cell, we had to use a battery of tests. One of our criteria was
the low contrast threshold for an optimal achromatic stimulus,
usually, a single moving bar or a ¯ashing spot. It has been shown that
the contrast sensitivity of the M cells in the dLGN is usually much
higher than that of the P cells (Kaplan & Shapley, 1982; Hicks et al.,
1983; Derrington & Lennie, 1984; Shapley, 1990). Indeed, P cells
rarely respond to sine wave gratings of less than 10% contrast,
whereas M cells often respond to contrasts as low as 1±3% (Hicks
et al., 1983; Shapley, 1990). Furthermore, neurons in the principal
magno-recipient layer 4Ca of the macaque striate cortex have high
luminance-contrast sensitivities while those in the principal parvorecipient layer 4Cb exhibit low luminance-contrast sensitivities.
(Blasdel & Fitzpatrick, 1984; Hawken & Parker, 1984; Tootell et al.,
1988; Hubel & Livingstone, 1990). However, because in virtually all
studies (e.g. Kaplan & Shapley, 1982; Hicks et al., 1983; Derrington
& Lennie, 1984; Shapley, 1990) the contrast sensitivity of parvo- and
magnocellular geniculate neurons was assessed on the basis of their
responsiveness to moving gratings while in the present study we have
assessed contrast sensitivity of cortical neurons on the basis of their
responsiveness to optimally oriented moving bars, we have conducted
additional control experiments by recording single neuron activity
from the parvocellular as well as from the magnocellular geniculate
layers and determining their achromatic contrast thresholds for single
bars. A small number of cells located in the intralaminar regions of
the dLGN, that is, the so-called koniocellular cells was also
examined.
The second test for revealing the presence of an M input to a
cortical neuron was based on the conduction velocity of their direct or
indirect geniculate afferents. Retino-geniculate M ®bres are faster
conducting than the retino-geniculate P ®bres (Dreher et al., 1976;
Schiller & Malpeli, 1978). Furthermore, the geniculo-cortical M
®bres are faster conducting than the geniculo-cortical P ®bres (Bullier
& Henry, 1980). We have ascertained whether a cell had an
excitatory M input or not, by measuring the difference in the
orthodromic latencies of the responses of cortical neurons to single
electrical stimuli delivered by electrodes placed in the optic radiation
(OR) in close proximity to the dLGN and in the optic chiasma (OX).
The latency difference of responses resulting from electrical stimulation of OX and OR sites re¯ect the conduction times of the retinogeniculate ®bres relaying through the dLGN and, as mentioned
above, these are distinctly different for the M and P pathways.
One more test that we used to reveal the presence of P and M
inputs to a cortical cell was to compare the cell responses to
isoluminant chromatic contours and achromatic luminance contours
moving at different velocities. Geniculate M cells respond well to
achromatic contours moving across their receptive ®elds at velocities
substantially higher than those which are effective in activating P
cells in the dLGN (Dreher et al., 1976). This means that a striate cell
can be presumed to receive converging P and M inputs, if it exhibits
more vigorous responses to isoluminant chromatic stimuli at velocities much slower than those which are most effective for achromatic
stimuli.
Preliminary reports describing our results have been published in
the form of abstracts (Vidyasagar et al., 1998a, b; Vidyasagar &
Dreher, 2002).
Materials and methods
Animals and preparation
The data for this study were gathered from nine macaques (six
Macaca fascicularis and three Macaca nemestrina) obtained from the
University of Melbourne/National Health and Medical Research
Council Macaque Facility. All procedures were approved by the
Australian National University's Animal Experimentation Ethics
Committee (constituted as per the ACT Animal Welfare Act 1992)
and conformed to the guidelines of the Australian Code of Practice
for the Use of Animals for Scienti®c Purposes and of the National
Institutes of Health, USA.
The monkeys (seven males, two females, weighing 2.7±7.0 kg)
were anaesthetized for initial surgery with i.m. injection of a mixture
of ketamine (10±16 mg/kg; Ketamil, Troy Laboratories, NSW,
Australia) and xylazine (3 mg/kg, Rompun, Bayer, Germany).
Following venous and tracheal canulations, paralysis of striated
muscles was induced with a single intravenous dose of 40 mg of
gallamine triethiodide (Flaxedil, May & Baker, England) and
maintained throughout the rest of the experiment with a continuous
intravenous infusion 10 mg/kg/h of gallamine triethiodide. From then
on, the animals were arti®cially respired and stable anaesthesia and
complete analgesia was maintained by the administration of sodium
pentobarbitone (1±1.5 mg/kg/h, Nembutal, Merial Australia, NSW,
Australia) and 70% nitrous oxide (in a 70 : 29.2 : 0.8 mixture of
N2O : O2 : CO2). Pressure points were in®ltrated with a long acting
local anaesthetic (Xylocaine, Astra). The electrocardiogram (ECG),
electroencephalogram (EEG), subscapular temperature and end-tidal
CO2 were continuously monitored. The body temperature was
thermostatically maintained around 36±37 °C with an electric heating
blanket, while end-tidal-CO2 was maintained around 3.6% by
adjusting stroke volume and/or the ventilation rate of the pulmonary
pump. To ensure adequate level of anaesthesia, the ECG and EEG
were carefully monitored and additional single small (4±10 mg)
doses of sodium pentobarbitone was injected intravenously when
necessary.
The pupils were dilated with topical application of 1% atropine
sulphate (Sigma, Vic., Australia). Hard (four animals) or airpermeable soft (®ve animals) contact lenses were used to protect
the corneas and refraction was corrected by additional lenses placed
in front of the eyes. In the case of hard contact lenses, to enable the
corneas to recover from any inadequate oxygenation, the contact
lenses were removed and eyelids kept closed for at least 6 h each
night and for shorter periods during the day. This maintained the
optics of the eyes in a very good condition throughout the length of
each experiment, which usually lasted 5±8 days. Arti®cial pupils,
ã 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 945±956
Convergence of geniculo-striate streams in macaque
4 mm in diameter and centred on the visual axis, were used routinely.
The optic discs and the foveolae were back projected using a fundus
camera on a tangent screen located 1 m from the animal. To be able
to determine precise locations of receptive ®elds in relation to the
fovea centrales, this procedure was conducted 2±3 times each day.
Electrophysiology
In seven animals a craniotomy was performed over the extrafoveal
representation in the striate cortex and a cylinder was cemented
around it. In three animals a craniotomy was performed over the
extrafoveal representation in the dLGN (in one of these animals we
recorded from both the dLGN and the striate cortex). The coordinates
of all craniotomies were based mainly on the atlas of Winters et al.
(1969). For dLGN recordings, this was usually 2±6 mm anterior and
9±12 mm lateral in Horsley-Clark co-ordinates and we used the
known topographical maps of Connolly & Van Essen (1984) to home
in on dLGN cells between three and ten degrees of eccentricity. For
cortical recordings, a large posterior cranial opening was made, the
lunate sulcus identi®ed and the penetrations made at least 3 mm
caudal to the sulcus and suf®ciently medial to be at least three
degrees from central foveal representation (Van Essen et al., 1984). A
plastic cylinder was then cemented around the craniotomy. In cases of
recordings from the striate cortex, a small hole was cut into the dura
just large enough to let in a tungsten-in-glass microelectrode and
recordings were made using a conventional AC-coupled ampli®er.
After positioning of the electrode just above the visual cortex, 2%
agar was poured into the chamber. In cases of recordings from the
dLGN, after cutting the dura, a tungsten-in-glass microelectrode was
®rst advanced rapidly to approximately 15 mm below the surface of
the cortex and then more slowly.
For recordings from the cortex, concentric bipolar stimulating
electrodes were also positioned, one in the optic radiations (OR) just
above the dLGN in the recording hemisphere and two more on either
side of the optic chiasma (OX), approximately 1 mm from the
midline. For recordings from the dLGN, stimulating electrodes were
inserted only into the OX. The mediolateral and rostrocaudal
positions as well as the depth of all the electrode tips were adjusted
until a vigorous response to ¯ashing photic stimuli could be recorded
through these electrodes.
Visual stimulation
Stimuli were produced on a Barco (Barco Industries, Belgium) colour
monitor controlled by a PC with a Vistaboard (Truevision, USA).
Most stimuli (moving bars or ¯ashing spots) were presented on a
white background (Illuminant C) of 6.3 candelas/m2. All stimuli were
calibrated to lie at one of four different saturation levels (three of
these shown in Fig. 1) in the MacLeod-Boynton isoluminant colour
space (MacLeod & Boynton, 1979) as formalized by Derrington et al.
(1984). The colour vector is given by the angle f, with 0±180 °
representing the LM-cone varying axis and 90±270 ° the S-cone
varying axis. We used a total of 32 points on the high saturation
ellipse (Fig. 1) at approximately equal angular distances. The CIE
coordinates of 16 of these were identical to or very close to the 16
used by DeValois et al. (1997). We have used a further 80 points at
three lower saturation levels. For achromatic stimuli, we varied the
luminance along a line perpendicular to the colour space at Illuminant
C (at x/y CIE coordinates of 0.31/0.316). For achromatic bar stimuli,
the luminance contrast was de®ned as the difference between bar and
background luminance divided by the background luminance (multiplied by 100 to express as percentage contrast). For gratings, contrast
was de®ned as (Lmax ± Lmin)/(Lmax + Lmin), again multiplied by 100
to express as percentage contrast. Note that with this convention, the
947
difference between Lmax and Lmin for a bar will be only half that of
the grating for equivalent contrast percentages. In measuring contrast
sensitivity, we usually used at least eight steps between 3% contrast
and 100%.
After initially optimizing stimulus orientation, colour, bar width
and velocity using hand-held stimuli, ®rst coarse (20° steps) and then
most often ®ne (5 or 10° steps) orientation tuning curves were
performed using optimal colour, bar size and velocity. Bar size and
velocity were optimized by short iterative runs using computer
generated stimuli ranging in bar widths from 0.1° to 2° and in
velocities from 0.35 °/s to 22.4 °/s.
Our criterion of response below 10% contrast to achromatic bar
stimuli as indicating M inputs was probably very conservative. The
classical data on contrast sensitivity of P and M dLGN cells was
based on their responses to grating stimuli (Kaplan & Shapley, 1982;
Hicks et al., 1983). In order to compare the responses of cortical cells
to bars and spots of isoluminant hues and to prevent confounding
effects from large surround stimuli we had to use bar or spot stimuli.
Therefore, in the present study in order to establish a baseline data for
classifying cortical cells on the basis of their contrast sensitivities we
measured contrast sensitivities to bars or spots of cells recorded from
the histologically identi®able parvo-, magno- and konio-cellular
layers of the dLGN. The lower bound of the 90% con®dence interval
was used to identify the two presented contrasts between which the
mean response became signi®cantly and consistently greater than the
level of spontaneous activity. The threshold was de®ned as the
contrast at which a line through the lower bounds of the 90%
con®dence intervals of the responses at these presented contrasts
intersected the mean spontaneous activity. For cells where the
con®dence interval of responses could not be reliably determined, the
threshold was de®ned as the contrast at which the best linear or
quadratic ®t through the mean responses (or subset of responses) from
all presented contrasts intersected the mean spontaneous activity.
Contrast sensitivity was then calculated as the reciprocal of the
contrast threshold.
Histology
The reconstructions of the laminar locations of cells recorded from
the striate cortex or dLGN, was aided by several electrolytic lesions
made along each recording track. Lesions were made by passing
current (6 mA for 6 s) through the recording microelectrode (with
microelectrode tip negative). At the end of each experiment, the
monkeys were deeply anaesthetized with an intravenous injection of
240 mg of sodium pentobarbitone and perfused transcardially with
1 L of a phosphate buffered saline solution followed by 2 L of 4%
neutral buffered formol saline. After removal of the brain from the
skull, the occipital cortices or thalami including dLGNs were frozen
sectioned (50 mm) and stained with neutral red. The position of
recorded cells was reconstructed with the aid of a drawing tube
attached to the microscope.
Results
General
The receptive ®elds of all 115 visual cortical cells in our sample were
located three to six degrees from the centres of the fovea. For a total
of 77 cortical cells, we were able to reliably identify P and/or M
signatures using all or a subset of our battery of tests. For all the
visual tests, we used stimuli that were optimized for orientation, bar
size and velocity. Orientation selectivity was ®rst tested with handheld stimuli and in 56 cells, we determined orientation tuning curves
ã 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 945±956
948 T. R. Vidyasagar et al.
FIG. 1. Diagram showing the locations in the 1931 CIE chromaticity scheme of three of the four saturation levels used in our experiments. The most
commonly used stimuli were in the outermost ellipse, corresponding to the highest saturation level. There were 32 points on each of the saturation levels,
corresponding to the same 32 different hues. The x/y coordinates of 16 of the 32 colours on the highest saturation ellipse were identical to or very close to
the 16 points in the diagram used by DeValois et al. (1997). The other three ellipses (the medium and medium-low saturation levels are shown in the ®gure)
were adapted from Bartleson (1977) and Wyszecki & Stiles (1982). The L- and M- cone varying axis (0±180°) and the S-cone varying axis (90±270°)
intersect at Illuminant C, which was the background against which the stimuli were presented. The corners of the triangle (R, G & B) represent the x/y
coordinates of the monitor's phosphors. The intersections of the colour vectors mentioned in Figs 2±4 with the highest saturation ellipse give the exact x/y
coordinates of the colours used in those runs.
quantitatively, using either achromatic light or dark bars, usually of
30% contrast or an isoluminant bar of optimum hue in cells that
responded poorly to the achromatic bar. In these 56 cells, we also
completed spectral selectivity measurements and contrast sensitivity
functions. We found that none of the 56 cells tested quantitatively
gave an equally strong response to all orientations (unoriented cells).
Cells which gave appreciable responses at all nonoptimal orientations
were considered as orientation-biased, while cells which did not
respond at all at some range of nonoptimal orientations were
considered to be orientation-selective. On this basis, we classi®ed 25
cells as orientation biased and 31 as orientation selective.
In a number of cells (10), even though they were extensively tested
and appeared to show some visual responses, we were unable to
reliably identify P and/or M signatures, because the responses were
poor, highly variable or we could obtain a signi®cant response only
when very high luminance contrast was added to a particular colour
contrast. We have identi®ed the latter type of cells also in the dLGN
(Vidyasagar & Dreher, 2002), which is the subject of ongoing studies.
For the 81 (out of the 115) cells for which binocularity was tested,
35 could be photically activated only via one eye (monocular cells
belonging to classes 1 and 7 of Hubel & Wiesel, 1962) while 46 cells
could be photically activated through either eye (binocular cells
belonging to classes 2±6 of Hubel & Wiesel, 1962). Latencies to
electrical stimulation of the optic chiasm and the optic radiations
were tested in 23 cortical cells, of which six could not be driven
electrically. Of the 17 cells for which we obtained latency data, 11
were in layer 4, ®ve in layer 5 and one at the bottom of layer 3. Six of
the 17 cells exhibited an OX-OR latency difference consistent with
the presence of a magnocellular input, namely 1.6 ms or less; ®ve of
these six cells were in layer 4Ca and one in layer 5. The other cells
all had OX-OR latency differences between of 2 and 3.9 ms.
Evidence for a lack of P and M convergence in a subset of
single units in V1
Figure 2 illustrates responses to chromatic isoluminant or achromatic
optimally oriented moving bars characterizing the clear majority of
V1 cells in which we were able to reveal either pure P or pure M
signatures, very similar to the typical parvocellular and magnocellular
responses seen in the dLGN (Kaplan & Shapley, 1982; Hicks et al.,
1983; Derrington & Lennie, 1984; Shapley, 1990). The cell whose
responses are illustrated in Fig. 2A responds well to isoluminant
stimuli of a particular spectral composition but not at all to
achromatic stimuli. On the other hand, the cell whose responses are
shown in Fig. 2B and C responds well to achromatic luminance
contrasts, but not at all to any of the isoluminant hues. Those cells,
which had a contrast sensitivity of eight or more, were considered
ã 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 945±956
Convergence of geniculo-striate streams in macaque
949
FIG. 2. Examples of responses of striate cortical cells to isoluminant chromatic and achromatic luminance stimuli. Peristimulus time histograms (PSTHs) were
based on responses to optimally oriented moving bars (10° 3 1°; 5.6 °/s); Bin width for the PSTHs in A, B and C was 16 ms. Number of sweeps: 8 in A, 5
in B and 4 in C.The colour vectors of the isoluminant chromatic stimuli are shown either on the left (A) or on the right (B). The exact x/y coordinates of
these can be obtained from the intersection of these vectors with the high saturation ellipse of Fig. 1. Note that according to our criteria (good response to
particular isoluminant chromatic stimuli, poor, if any, response to achromatic contrast), the layer 4Cb cell whose responses are illustrated in A appears to
receive a pure parvocellular input. By contrast, the 4Ca simple-like cell whose responses are illustrated in B and C appears to receive a pure magnocellular
input (no response to isoluminant chromatic stimuli, achromatic contrast threshold below 10% and response saturates at 30% contrast).
most likely to be receiving a magnocellular input. We adopted this
criterion on the basis of our geniculate data (summarized in Fig. 5A)
when using moving bar or ¯ashing spot stimuli as per our de®nition
of contrast (see Materials and methods). The dLGN parvocellular
cells had a mean contrast sensitivity of only 2.95 (Fig. 5A;
SE 6 0.37; n = 33), with only one cell showing a sensitivity above
ten and with only three cells with a contrast sensitivity better than six.
On the other hand, the magnocellular dLGN cells had a mean contrast
sensitivity of 11.85 (Fig. 5A; SE 6 1.23; n = 18), with only one cell
having a contrast sensitivity below six and only six cells exhibiting
contrast sensitivity below ten. Another seven cells (no examples are
shown here) had poor contrast sensitivity similar to the parvocellular
dLGN cells recorded by us, but did not show any spectral selectivity.
We assume that these cells receive inputs from achromatic
parvocellular cells, which form a small subset of parvocellular cells
(6/33 in our sample, see also Wiesel & Hubel, 1966; Dreher et al.,
1976; Reid & Shapley, 2002).
Evidence for P and M convergence in a subset of V1 single
neurons
As noted earlier, we took the presence of a response to isoluminant
stimuli and associated spectral selectivity as a clear indication of a
parvocellular input. Unlike in the dLGN where the koniocellular (K)
and parvocellular (P) cells are segregated in separate laminae or
distinct interlaminar regions, at the cortical level, there is no de®nite
way of distinguishing P inputs from the K input. Therefore, at this
stage we have ignored the possibility that some of the cells, which we
had identi®ed as receiving P input, could actually have received K
inputs. As the contrast sensitivity of the koniocellular cells in our
sample of dLGN cells (Fig. 5A; mean 3.25 6 0.56; n = 11) was not
signi®cantly different from that of dLGN parvo cells (t-test; P > 0.1)
but signi®cantly different from that of dLGN magno cells (t-test;
P < 0.0001), the inclusion of any cell with a konio input is unlikely to
compromise our contrast sensitivity criterion for identifying a
magnocellular input.
Our criteria for identifying a magnocellular input to a cell
depended upon more than one parameter. The latency of the
responses of cortical neurons to electrical stimulation along the
retino-geniculo-cortical pathway is a reliable indicator of the
conduction velocity of the afferents when the cortical cells receive
an afferent drive strong enough to be suprathreshold for spike
generation. Because the M and P channels relay strictly in parallel
through the dLGN, when the cortical neuron exhibited a latency
difference between the optic chiasma and the optic radiation (just
above the dLGN) stimulation that was 1.6 ms or less, we considered
it as an unequivocal indication of an excitatory M input to the cortical
cell (Dreher et al., 1976). On the other hand, Dreher et al. (1976)
were recording from the dLGN, in which case, the latency to
electrical stimulation from the optic chiasma incorporates only one
synapse, unlike the minimum of two synapses in our case. This
introduces signi®cant latency jitter and increases failure rate in
successful spike transmission across all the relevant synapses.
ã 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 945±956
950 T. R. Vidyasagar et al.
FIG. 3. Responses of two striate cortical cells (A and B) to isoluminant chromatic and achromatic (luminance) contrasts. Stimuli were optimally oriented
moving bars (A, 11° 3 0.3°, 1.4 °/s; B, 8° 3 0.3°, 0.7 ° /s). The colour vectors of the isoluminant chromatic stimuli are shown on the left. Bin width for the
PSTHs was 40 ms. Number of sweeps for all PSTHs was 4. Note that the layer 6 complex cell shown in A exhibits not only responses to a broad range of
isoluminant stimuli except blue-green and green (P input), but also high achromatic contrast sensitivity (M input). Similarly, the layer 5 cell in B not only shows
selectivity to red isoluminant stimuli, but also fairly high contrast sensitivity; this cell also yielded OX-OR latency difference compatible with an M input.
Therefore, in those instances where the latencies from each stimulation site had appreciable jitter, but nevertheless encompassed a
possible latency difference of 1.6 ms or less, we have taken the
luminance contrast sensitivity data into account. In these cases, if the
cell was responding to stimuli of 10% (or less) luminous contrast, it
was taken as an indication that the cell had a magnocellular input.
However, outside of layer 4, electrical stimulation sites in the
geniculo-cortical segment very rarely produce action potentials of
cortical neurons (Bullier & Henry, 1980) and almost never in relation
to the retino-geniculate segment (Dreher et al., 1976). Even though
we found both simple like and complex like cells in all categories, the
sample sizes are too small to make a statement about their
distribution.
Figures 3 and 4 show responses of three cells which appeared to
receive both parvocellular and magnocellular inputs. Thus the layer 4
cell, whose responses are illustrated in Fig. 3A, responded well to
moving bars of a broad range of colours (yellow, red, purple and
blue), but did not show any response to blue-green or green
isoluminant stimuli. The cell was also very sensitive to yellow and
red bars, exhibiting vigorous responses even to stimuli of lower
saturations than those presented in the ®gure. At the same time, the
cell was very sensitive to achromatic luminance contrasts responding
well to moving elongated achromatic contrasts of 6%. We conclude
therefore that this cell received effective inputs from both M and P
channels.
The layer 5 cell whose responses to visual stimuli are shown in
Fig. 3B exhibited response-latency difference for electrical stimuli
delivered to the OX and those delivered to the OR (just above the
dLGN) of 1.6 ms. Thus, on the basis of this OX-OR latency
difference this cell appeared to receive a suprathreshold excitatory
magnocellular input. Consistent with this, the response threshold to
achromatic visual stimuli was close to 10% contrast. At the same
time, the cell showed good chromatic selectivity responding well to
moving red bars. It showed an ON response to red bars and an OFF
response to blue, blue-green and green stimuli. This colouropponency clearly suggests the presence of a parvocellular input to
the cell (see Discussion).
Figure 4 shows the responses to different visual stimuli of a cell
recorded from layer 4 Ca. This cell was tested with chromatic stimuli
(blue and yellow stimuli on isoluminant white background) and
luminance (achromatic) stimuli moving at different velocities across
the cell's receptive ®eld. At the lower velocities (0.7 and 1.4 °/s), the
ã 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 945±956
Convergence of geniculo-striate streams in macaque
951
FIG. 4. Responses of an orientationally biased, striate cortical cell from layer 4Ca to optimally oriented chromatic and luminance contrast bars (5.5° 3 0.15°)
moving at four different velocities. The yellow bar's colour vector was 310° and that of the blue bar's 130°. The bin widths for the four velocities (in
ascending order) were 80, 40, 20 and 5 ms. Number of sweeps for the four velocities were 4, 8, 4 and 8, respectively. The y scales have been individually
adjusted for each PSTH to provide a common scale bar as shown in the middle. Note that at lower velocities (0.7 and 1.4 °/s), the cell's response to
chromatic contrast is more marked than that to luminance contrasts. With increasing velocity, the cell shows greater response to luminance contrasts than to
chromatic contrasts, indicating that the balance of P and M inputs varies with the velocity.
cell's response to chromatic contrast was more marked than that to
luminance contrasts. However, with increasing velocity, the situation
gradually reversed and at the highest velocity tested (11.2 °/s) there
was a good response to luminance contrast and little response to
chromatic contrast. This velocity related reversal of the relative
magnitudes of the responses to chromatic and achromatic stimuli
strongly suggests to us that the cell received excitatory inputs from
both P and M channels (see Discussion).
Comparison of preferences for luminance and colour
Johnson et al. (2001) have used a sensitivity index to quantify the
extent to which a cell prefers chromatic or achromatic stimuli, which
they found to be very useful in classifying cells recorded from area 17
of macaque monkeys. The index they used was the ratio of the peak
responses to equiluminant and achromatic (luminance) grating
stimuli. We have used a similar index for our nonperiodic stimuli
(bars and spots but mostly bars), namely
sensitivity index = responsemax(equiluminat)/responsemax (luminance).
It should be stressed that the actual values obtained by us cannot be
directly compared to those of Johnson et al. (2001), because the
stimuli we used are different from those of Johnson et al. (2001) and
also we have not equated the chromatic and achromatic stimuli for
cone contrast. The latter is neither possible nor advisable in our case
because we use a large range of isoluminant hues to ®nd the optimum
hue for each cell and the cone contrast will be very different for these
stimuli. So there cannot be a single cone contrast value for luminance
stimuli that can be used legitimately across all the cells. On the other
hand, to be able to classify our cortical cells that have a range of hue
preferences on the basis of their responses to an achromatic stimulus,
it is necessary to use the same luminance contrast across the whole
population. For these reasons, we have used a 100% light or dark
aperiodic stimulus on our background of 6.3 candelas/m2 as the
achromatic stimulus to calculate the sensitivity index for all dLGN
and cortical cells. The chromatic stimulus chosen for each cell was
the isoluminant stimulus on the white background (Illuminant C;
6.3 candelas/m2) that gave the best response among all the
isoluminant stimuli.
Figure 5 summarizes the result of this analysis for the 62 dLGN
cells and 56 striate cortical cells for which we had reliable data on
both sensitivity index and contrast sensitivity. On the abscissa, data
points to the left represent cells with strong achromatic responses in
comparison to isoluminant chromatic responses (typical magnocellular) and towards the right, the data points represent cells with
vigorous responses to the appropriate isoluminant colour contrasts but
with poor responses to even high achromatic contrasts. It can be seen
clearly that in dLGN, cells from the parvocellular laminae tend to fall
low and to the right, whereas the magnocellular cells tend to have low
sensitivity indices but fairly high contrast sensitivity. We could
unequivocally localize 11 cells in the koniocellular layers. Of these
three were classi®ed as achromatic, three exhibited blue/yellow
ã 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 945±956
952 T. R. Vidyasagar et al.
FIG. 5. Achromatic contrast sensitivity is plotted against sensitivity index (ratio of equiluminance response to luminance response) for 62 dLGN cells (A) and
56 striate cortical cells (B). Parvo, konio and magno data points in A refer to cells that were identi®ed on histological grounds to be in parvo-, konio- or
magnocellular layers of the dLGN, respectively. P, M and P/M data points in B were classi®ed according to the functional criteria explained in the text. The
cells with a zero sensitivity index are those that showed no response at all to any isoluminant chromatic contour that we regularly used. The small numbers
beside some of the data points are added to indicate the number of overlapping data points. Some of the cortical cells identi®ed as receiving P inputs may be
receiving alternatively (or in addition) K inputs. See Discussion for further clari®cation of this point.
opponency and ®ve showed red/green opponency. This sample is
however, too small to make any generalizations about the functional
properties of the K layers in the macaque dLGN and it will have to
await the results of ongoing studies. Furthermore, our identi®cation of
koniocellular cells has to remain tentative, as it was based on
histological reconstruction of electrode tracks in sections stained for
Nissl substance rather than for immunocytochemistry.
There were practically no cells that had a fairly high contrast
sensitivity similar to the typical M cells, but with a SI anywhere close
to 1 or higher. However, in the cortex, we found a clear new cell
group that combined these two features. Cells constituting this new
group (referred to as P/M cells in Fig. 5B) formed approximately
32% (18/56) of this cortical sample.
Proportion and laminar distribution of cells receiving P, M and
P/M inputs
Out of the 77 cells where we could come to a de®nite conclusion about
whether P and/or M inputs were present using one or more of our criteria
for M inputs, 41 cells (53% of the sample) appeared to receive only a
parvocellular input, 16 cells (21% of the sample) appeared to receive
only a magnocellular input and 20 cells (26% of the sample) appeared to
receive both P and M inputs. Among the P/M cells, nine showed blue/
yellow opponency and the rest showed red/green opponency. Among
the 41 cells that seemed to receive a pure P input, 17 exhibited red/green
opponency, 17 showed blue/green opponency and seven were classi®ed
as receiving an achromatic P input.
ã 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 945±956
Convergence of geniculo-striate streams in macaque
We were able to identify unequivocally the laminar location of 62
of these cells. The cells showing mixed inputs were found in all
layers except layer 1. Thus, out of the 12 cells recorded from the
supragranular layers 2/3 (12/62; 19.4% of the sample), ten appeared
to be driven exclusively by P inputs and two appeared to receive both
P and M inputs. Over 30% (19/62) of cells with identi®ed P, M or
mixed P/M input were recorded from layer 4 (seven of those cells
were found in parvo-recipient layer 4Cb, four cells were recorded in
the magno-recipient layer 4Cα and eight cells were located in layer
4B). Six of these cells (all of them located in layer 4Cβ), appeared to
receive a pure P input, eight received a pure M input (three of them
were located in layer 4Ca and ®ve in layer 4B) while the remaining
®ve cells appeared to receive mixed P and M inputs (one of them was
located in layer 4Cb one in layer 4Ca and three in layer 4B). Finally,
half of the sample (31/62) were located in the infragranular layers 5
and 6 (20 were driven by P channel, four were driven by M channel
and seven appeared to receive both P and M inputs).
Discussion
Our results suggest that majority of cells in the striate cortices of
macaque monkey (like virtually all cells in macaque's dLGN; cf. for
review Kaplan et al., 1990; see also present control experiments)
receive their suprathreshold excitatory input either from the
parvocellular (P) or from the magnocellular (M) channels. Indeed,
most cortical cells in our sample of cortical neurons fall into two
distinct categories. One group of cells (like cells in the parvocellular
layers of the dLGN) exhibited poor contrast sensitivity (contrast
thresholds usually well over 10%) to moving optimally oriented
achromatic bars and clear-cut responses to isoluminant stimuli of
particular spectral compositions. The other group (like cells in the
magnocellular layers of the dLGN) exhibited good contrast sensitivity
(threshold 10% or less) to moving optimally oriented achromatic bars
but poor responses to isoluminant stimuli of any of a range of spectral
compositions. However, a substantial proportion of cortical neurons
appear to receive suprathreshold convergent excitatory inputs from
both the magnocellular and parvocellular channels. Our argument is
based mainly on the presence in our sample of a proportion (26%) of
cells which exhibited high contrast sensitivity (10% or less) to
moving optimally oriented achromatic bars (presumed M input) and/
or retino-geniculate conduction velocity measurements consistent
with a magnocellular input combined with clear-cut responses to
isoluminant stimuli of particular spectral composition (presumed P
input).
Some would argue that the high contrast sensitivity to achromatic
gratings combined with clear-cut responses to isoluminant stimuli
does not indicate a convergence of M and P channels on a particular
cortical cell but re¯ects excitatory convergence and probability
summation of a very large number of parvo inputs (e.g. Merigan &
Eskin, 1986; Sclar et al., 1990; Watson, 1992). This argument is
partially supported by the ®nding (Merigan et al., 1991) that
behavioural contrast sensitivity for higher spatial frequencies was
reduced after ibotenic acid lesions restricted to the geniculate
parvocellular layers, but not after ibotenic acid lesions restricted to
magnocellular layers. Although we cannot entirely exclude the
possibility of probability summation, there are several lines of
evidence, which argue against it. First, a proportion of cells which
exhibited high achromatic contrast sensitivity and clear-cut responses
to isoluminant chromatic stimuli also responded to electrical
stimulation of optic chiasma and optic radiation with latencies
indicating unequivocally magnocellular conduction velocity of their
953
retino-geniculo-cortical afferents. Second, the probability summation
is not apparent in a majority of cortical neurons which either exhibit
poor contrast sensitivity (with contrast thresholds usually well over
10%) to moving optimally oriented achromatic bars and clear-cut
responses to isoluminant chromatic stimuli (cells which appear to
receive only the parvocellular input) or good contrast sensitivity
to moving optimally oriented achromatic bars but poor responses to
isoluminant chromatic stimuli (cells which appear to receive only the
magnocellular input). Indeed, the achromatic contrast thresholds of
cortical cells which appear to receive their input from the magnochannel is not consistently lower than that of most moderately
sensitive magnocellular dLGN cells and never as low as that of the
most sensitive magno cells reported in the literature (e.g. Kaplan &
Shapley, 1982; Hicks et al., 1983; Derrington & Lennie, 1984;
Shapley, 1990). Third, Lee et al. (1995) have shown that in the
context of a vernier acuity task at low contrasts, the poorer positional
signal from the P cells cannot be compensated for by their higher
sampling density. Fourth, selective and reversible pharmacological
inactivation (using electrodes containing 25 mM solution of gaminobutyric acid) of one of the magnocellular layers in the dLGN
of another primate (bush baby ± Galago crassicaudatus) resulted in
signi®cant elevations in contrast thresholds of all tested cells in
visuotopically corresponding part of area VI as well as a substantial
reduction in the magnitude of responses of cortical neurons at each
stimulus contrast (Allison et al., 2000). Although selective inactivation of the parvocellular dLGN layer of bush babies signi®cantly
reduced the average peak response amplitude of cells in visuotopically corresponding part of area V1, it did not elevate their average
contrast threshold (Allison et al., 2000). These results provide strong
support for the idea of convergence of P and M inputs onto single V1
neurons in the Galago. Furthermore, Kaplan et al. (1990) have shown
that the degree of P cell convergence required for probability
summation effectively increasing the contrast sensitivity of the P
system is too high to be supported by the known anatomical and
physiological data for the extent of geniculocortical convergence.
Alternatively, one could argue that virtually all cortical cells,
which we have identi®ed as receiving both P and M inputs, receive
only M input. Thus, it has been reported in the past that a proportion
of magnocellular cells recorded from macaque's dLGN are the socalled Type IV which exhibit colour opponent surrounds (Wiesel &
Hubel, 1966; Dreher et al., 1976; Reid & Shapley, 2002).
Furthermore, macaque's ganglion cells which project to the
magnocellular dLGN layers exhibit residual responses to equal
luminance borders (Valberg et al., 1992) which are analogous to the
second harmonic responses of those neurons to heterochromatically
modulated lights (Smith et al., 1992). Indeed, moving isoluminant
chromatic bars which we have used to stimulate cortical neurons were
sometimes large relative to the typical size of receptive ®eld centres
of cortical cells from which we recorded and could potentially
involve colour opponent surrounds. Finally, one can not be certain
that our isoluminant stimuli determined for central vision of human
observers coincide with the isoluminant planes of all macaque
magnocellular cells. There are however, at least three lines of
evidence, which argue against that line of criticism. First of all, none
of the magnocellular cells recorded by us in the dLGN exhibited
clear-cut responses to large moving isoluminant chromatic bars.
Second, we have deliberately tested the cortical cells showing pure
magnocellular inputs with very wide bars (e.g. 10° 3 1° bar for the
cell shown in Fig. 2B and C) and we have not seen any noticeable
responses to our range of isoluminant chromatic stimuli. Third, at
least one of the cortical cells, which we identi®ed as receiving both M
and P inputs, was located in the parvo-recipient layer 4Cb.
ã 2002 Federation of European Neuroscience Societies, European Journal of Neuroscience, 16, 945±956
954 T. R. Vidyasagar et al.
There are several lines of evidence suggesting that in reality, the
percentage of cortical cells receiving a convergent suprathreshold
excitatory input from both magno and parvochannels could be higher.
(i) The electrical stimulation technique is helpful in instances when
action potentials can be reliably evoked in the cortical cell from
different stimulating points along the afferent pathway. However,
there were a number of cortical cells where we were unable to evoke
action potentials from at least one of our stimulating electrodes (cf.
also Dreher et al., 1976; Bullier & Henry, 1980). (ii) Our contrast
sensitivity criterion for M inputs, as explained earlier, was very
conservative. (iii) The cells classi®ed as having pure M inputs, though
showing no spectral selectivity, could still have a spectrally balanced
parvocellular input that could not be demonstrated by our test using
isoluminant stimuli. However, the impact of some of the unclassi®ed
cells on the percentages is unpredictable. Some of these cells, though
tested adequately, showed neither a clear P nor an M input.
With these caveats in mind, we reserve any quantitative claims
about the exact degree of convergence of M and P channels to more
exhaustive studies that are underway. However, it is clear from the
present data that there is a possible functional convergence of P and
M channels on single neurons in the macaque striate cortex. Such
convergence is consistent with earlier reports from other laboratories
(Malpeli et al., 1981; Nealey & Maunsell, 1994; Sawatari &
Callaway, 1996, 2000; Yabuta & Callaway, 1998; Yabuta et al.,
2001) in which techniques quite different from ours were used. We
should however, add a cautionary note that the cells, which we
classify as having a P input, might include those receiving a
koniocellular input, if the blue-on cells form a separate koniocellular
pathway to the cortex in old world diurnal simian primates as has
been claimed for a new world diurnal simian, the common marmoset
(White et al., 1998).
In principle, there can be cortical cells with pure P inputs, but
lacking any spectral selectivity due to a convergence of two different
spectrally opponent types of dLGN cells and/or an input from a small
number of achromatic cells reported in the macaque dLGN (Wiesel &
Hubel, 1966; Dreher et al., 1976; Reid & Shapley, 2002). Therefore,
it would be appropriate to consider those cells failing on our tests to
show an M input, but not showing a response to any isoluminant
contours, as having, ipso facto, a parvocellular input. Surprisingly, we
rarely encountered such cells. This in turn suggests that most cells
with a pure P input show some spectral selectivity. This point
however, needs to be clari®ed in future studies.
Cells with inputs from both P and M channels were found in all
layers. That such cells were found in layer 4 is of special signi®cance.
The presence of these cells in layer 4 is consistent with more recent
anatomical data which provide a substrate for convergence of P and
M in layer 4C (Lund et al., 1994; Yoshioka et al., 1994; Levitt et al.,
1996) and models of cortical organization that assume such
convergence in the geniculate input layers (Bauer et al., 1999). The
presence of cells with mixed inputs in other layers might be either a
simple re¯ection of the mixing already occurring in layer 4 or may be
the result of yet another level at which convergence between the
different channels occurs within the striate cortex. It is also worth
noting that the convergence is seen for both classes of colour
opponent cells, as approximately half of the P/M cells showed red/
green input and the other half a blue/yellow input.
It is worth mentioning in this context that the excitatory
convergence of different visual information channels on single
neurons in the primary, as well as in the so-called higher-order visual
cortical areas, is a characteristic feature of another highly visual, but
nonprimate, mammal, the domestic cat (see for recent review Burke
et al., 1998).
The presence of convergent inputs from different information
channels in a substantial subpopulation of neurons in macaque's striate
cortex does not rule out the possibility that cells receiving either pure
M or pure P excitatory inputs form a subset of cells which project
exclusively to particular higher cortical or for that matter even
subcortical regions. Indeed, the separation of the higher cortical areas
into the dorsal stream receiving mainly the magnocellular input and the
ventral stream receiving mainly the parvocellular input might still be
largely valid. This may be especially true of the predominantly
magnocellular input to area V5/MT (Maunsell et al., 1990). Indeed, for
certain perceptual functions, it may be necessary to retain a separate
pathway, such as a fast magnocellular channel (Schmolesky et al.,
1998; Vidyasagar, 1998, 1999, 2001; Bullier et al., 2001) which might
mediate various modulatory functions, including feedback for
attentional purposes (Vidyasagar, 1998, 1999, 2001). The cells with
pure P inputs presumably underlie the predominance (e.g. Merigan &
Maunsell, 1993 for review) of the parvocellular channel in the ventral
stream. It is also not unlikely that the degree of convergence of P and M
inputs observed in macaque V4 neurons (Ferrera et al., 1992, 1994)
re¯ects the input from the P/M cells of striate cortex.
One might wonder what could be the function of convergence of
the two parallel streams. Such convergence may help in two ways.
First, as both luminance and chromatic differences in natural scenes
tend to occur together, the cells showing P and M convergence may
be better suited for rapid detection of such stimuli. Second, the
saliency of colours and chromatic borders can be increased by taking
advantage of the luminance differences that usually accompany
colour differences between objects. Keeping the channels separate
peripherally in the retina and geniculate may be part of the common
strategy of maximizing simultaneous representations of different
dimensions on a limited topographically organized surface that needs
to retain resolution and sensitivity (e.g. Vidyasagar, 1985). However,
with the extensive divergence at the striate cortical level, where there
are approximately 500 cells per retinal ganglion cell (calculated from
Creutzfeldt, 1993 and Peters et al., 1994), the P and M inputs could
be combined already in different ways to provide a range of very
effective feature detectors. In fact a continuum of spatio-temporal
properties of V1 cells (Kulikowski & Walsh, 1993) is consistent with
this hypothesis and its perceptual signi®cance (Kulikowski et al.,
1997).
Acknowledgements
We thank Dr G. H. Henry for helpful criticism and Ms J. Cappello and Mrs E.
Henry for technical assistance. The project was supported by a grant from the
National Health and Medical Research Council to T.R.V and B.D. J.J.K. was
supported by grants from the Royal Society of London and the John Curtin
School of Medical Research.
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