Cerveau et Vision, Institut National de la Santé et de la Recherche Médicale U371, 69675 Bron Cedex, France
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Hupé, Jean-Michel, Andrew C. James, Pascal Girard, and Jean Bullier. 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, 2001. We analyzed the extracellular responses of 70 V1 neurons (recorded in 3 anesthetized macaque monkeys) to a single oriented line segment (or bar) placed within the cell classical receptive field (RF), or center of the RF. These responses could be modulated when rings of bars were placed entirely outside, but around the RF (the "near" surround region), as described in previous studies. Suppression was the main effect. The response was enhanced for 12 neurons when orthogonal bars in the surround were presented instead of bars having the same orientation as the center bar. This orientation contrast property is possibly involved in the mediation of perceptual pop-out. The enhancement was delayed compared with the onset of the response by about 40 ms. We also observed a suppression originating specifically from the flanks of the surround. This "side-inhibition," significant for nine neurons, was delayed by about 20 ms. We tested whether these center/surround interactions in V1 depend on feedback connections from area V2. V2 was inactivated by GABA injections. We used devices made of six micropipettes to inactivate the convergent zone from V2 to V1. We could reliably inactivate a 2- to 4-mm-wide region of V2. Inactivation of V2 had no effect on the center/surround interactions of V1 neurons, even those that were delayed. Therefore the center/surround interactions of V1 neurons that might be involved in pop-out do not appear to depend on feedback connections from V2, at least in the anesthetized monkey. We conclude that these properties are probably shaped by long-range connections within V1 or depend on other feedback connections. The main effect of V2 inactivation was a decrease of the response to the single bar for about 10% of V1 neurons. The decrease was delayed by <20 ms after the response onset. Even the earliest neurons to respond could be affected by the feedback from V2. Together with the results on feedback connections from MT (previous paper), these findings show that feedback connections potentiate the responses to stimulation of the RF center and are recruited very early for the treatment of visual information.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
As in many other structures of
the visual system, the responses of neurons in area V1 can be modulated
by stimuli presented outside the "classical" receptive field (RF).
These modulations provide a comparison between stimuli inside and
outside the RF, a mechanism allowing the integration of local and
global information. For example, a proportion of V1 neurons gives a
stronger response to a single bar flashed in their RF and embedded in a
field of bars of orthogonal orientation flashed outside their RF, than to a bar surrounded by bars having the same orientation (Knierim and van Essen 1992). Perceptually, these stimuli are quite
distinct. The bar surrounded by bars of orthogonal orientation is more
salient, it "pops out" (Treisman and Gelade 1980
).
The center/surround properties of V1 neurons can therefore be part of
the neural basis of preattentive parallel processes. The automatic
character of such preattentive processes is in keeping with the fact
that the orientation-selective modulations by the surround can be
recorded in the neurons of anesthetized animals (Li and Li
1994
; Nothdurft et al. 1999
; Sengpiel et
al. 1997
; Sillito et al. 1995
).
The orientation-selective surround modulations are presumed to be
generated at the cortical level, as orientation selectivity first
appears in V1 (Hubel and Wiesel 1962). One possible
structural basis for such orientation-specific modulations is the set
of horizontal connections that link together neighboring neurons in V1.
Lateral long-range connections within V1 connect neurons with
nonoverlapping RF (Salin and Bullier 1995
), but they
preferentially connect neurons with similar orientation preferences
(Gilbert 1992
; Tamura et al. 1996
). As V1
RF are small, there is a need for numerous and extensive connections to
cover the whole extent of the surround of the RF, which can cover up to
10 times the size of the RF (Levitt and Lund 1997
).
Feedback connections from higher order areas are ideal candidates for
these modulations, as neurons of these areas have larger RF than V1
neurons and their projections display a high degree of convergence.
Contrary to feed-forward connections, feedback connections have been
described as nonvisuotopically organized, meaning that a given target
cell in V1 receives input from cells in higher areas having RFs
extending beyond that of the target cell (Salin and Bullier
1995; Salin et al. 1992
, 1995
). Feedback connections from V2 in the monkey (Barone et al. 1995
;
Rockland and Virga 1989
) are numerous: about 10 million
or more V2 axons project to area V1, and the mean degree of convergence
of area V2 afferents is high, perhaps more than 100 afferent axons per V1 cell (Budd 1998
). These connections convey
information concerning a region of visual field approximately five to
six times the size of the average V1 RF (Angelucci et al.
2000
).
The orientation-specific modulation of responses to center/surround
stimuli is observed 15-20 ms after the response onset (Knierim
and van Essen 1992; Nothdurft et al. 1999
).
Delayed modulations for textured surround of different orientations
have also been demonstrated in awake monkeys (Lamme
1995
; Zipser et al. 1996
). In these studies, the
delay was even larger (50-100 ms). As the responses of V2 neurons lag
the V1 responses by about 10 ms (Nowak et al. 1995
),
such a delayed modulation provides another argument suggesting that
orientation-dependent modulations depend on the feedback from V2.
Functional studies of cortico-cortical feedback connections are rare
(Salin and Bullier 1995). The only available data
concerning feedback influences on center/surround interactions in the
macaque monkey suggest that feedback from MT play a role in
figure/ground segregation (Hupé et al. 1998
). When
MT was inactivated, V3 neurons tested at low salience were no longer
suppressed by a background stimulus (extending far away from the RF)
moving coherently with a bar that swept across the RF. Even if
center/surround interactions were not directly studied in that paper,
the results suggested that feedback connections play a role in such
interactions. Similar results have been found in areas V2 and V1
(Bullier et al. 2000
).
We therefore decided to test whether center/surround interactions
observed in V1 neurons depend on the feedback from V2. We used stimuli
made of light bars flashed in and around the RF, to which the responses
of V1 neurons are well documented, and are similar in awake and
anesthetized monkeys (Knierim and van Essen 1992;
Nothdurft et al. 1999
). We tested surround suppression created by bars of similar orientation as the central bar, as well as
modulations of the response that depended on the orientation properties
of the surround.
In preliminary experiments, we had found that only a few V1 neurons
were affected by V2 inactivation. The effects observed on this small
sample were, however, unexpected. Two major effects could be observed:
a decrease of the response to a single bar in the RF and strong
increases to "surround-only" stimuli, i.e., stimuli made of bars
placed only in the surround and that did not elicit any response in the
control condition. In these cases, changes in the center/surround
responses were observed, but they followed the increases of response of
the surround-only stimuli and thus could be explained by linear
summation mechanisms and not by a change in the center/surround
interactions, which were never observed. These results have been
described in an abstract form (Hupé et al. 1997),
and one example has been published (Bullier et al. 1996
;
Payne et al. 1996
). We proposed a model that could explain these surprising results. The basic idea of this model was that
feedback connections from V2 gated the V1 intrinsic connectivity and
had virtually the power of modulating, but not shaping the center/surround interactions (Hupé et al. 1997
).
In these preliminary experiments, we had used three micropipettes
filled with GABA 100 mM to inactivate V2. Anatomical data indicated
that it was probably not sufficient to inactivate the whole extent of
the convergence zone of V2 to a given V1 neuron. We tested in our model
the effects of partial inactivation and found that it explained why we
had observed effects in only a few V1 neurons, and why the
surround-only responses were the predominant effect. We predicted that
if we were able to inactivate the whole feedback input from V2 to V1
cells, we should not only observe effects quite systematically, but we
should also see an equivalent proportion of effects (decreases) on the
center response and on the surround response (increases). The role of
feedback was therefore understood as a push-pull mechanism
(Bullier et al. 1996; Payne et al. 1996
).
Another possible explanation of the increases of the surround-only
responses was provided by recent results that show that the size of the
V1 RF depends on the state of the electroencephalogram (EEG) of
anesthetized animals (Wörgötter et al.
1998). As our preliminary experiments had been done without any
systematic control of the EEG during the control and inactivation
phases, it was possible, even if unlikely, that, among the great number
of tests that had been done, changes of the EEG had occurred precisely when GABA was injected. This could have lead to an increase of the RF
size, and thus the previously unresponsive surround stimulus now had
encroached on the RF, leading to the observed increases of response to
the surround only stimulus.
We therefore decided to undertake a new series of experiments with more extensive inactivation of V2 and a careful control of the EEG state of the animals before and during the V2 inactivation. In the present paper we describe results obtained in three monkeys where we carried out extensive inactivation of V2 by GABA under control of the EEG state. We did not find any increase of the response to the surround stimuli when V2 was inactivated. We also did not find any effect of feedback connections on the center/surround interactions. We nevertheless observed decreases of response to the center stimulus, as already reported in the preliminary experiments. These effects were observed from the very beginning of the visual response.
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Physiology
Recordings were obtained from three anesthetized and paralyzed
cynomolgus monkeys. Procedures were similar to those described in the
companion paper (Hupé et al. 2001). In addition,
we recorded the EEG and we calculated the fast Fourier transform
on-line to check the depth of the anesthesia and also to monitor,
on-line and off-line, the changes of the EEG states, especially within the 10- to 30-Hz range. We excluded some neurons from the analysis because of changes in the EEG state during the recording session (see
DISCUSSION).
We used window discriminators (Neurolog) to isolate multi-unit activity
from background in the V2 recordings. These recordings in V2 were done
to monitor the efficiency of the inactivation by GABA (Fig. 2). For V1
recordings, we used a spike discriminator (MSD, from Alpha Omega) to
extract single units and to monitor the identity of the neuron under
study during periods of control, V2 inactivation, and recovery. We did
not always record perfectly isolated neurons. In the case of multi-unit
recordings, we first verified that the isolation index (II) (see
Hupé et al. 2001) was similar in all the controls.
When the II was below 0.8, we were especially cautious. If we observed
some change during the V2 inactivation, we always tried to see whether
it was possible to explain it by a change in spike isolation. Several
attempts with different templates were even done if necessary, and the resulting peristimulus time histograms (PSTHs) were compared. We excluded some neurons from the analysis because of changes in
isolation. Some sites for which the isolation was close to 0 were
called "multi-unit" but were, however, kept for the analysis if the
II did not change. In addition, if the response of these multi-unit
clusters changed during the V2 inactivation, a special attention was
given to the stationarity of responses across controls and recovery,
and if these recordings were sufficiently similar, the site was then kept.
Data sampling
After the first stage rejections due to changes in EEG or isolation, the responses of 70 V1 neurons (28 single units, 17 poorly isolated units, and 25 clusters of 2-4 units) to 7 stimuli were analyzed.
The minimum discharge field (RF in this paper) was plotted with a hand-held ophthalmoscope. The RFs were all located between 2 and 3° from fixation, in the lower right quadrant. A high contrast bar (120 cd/m2, approximately 1 log unit above the background luminance) was optimized in size for each neuron. The length of the bar was between 0.1 and 0.8° (median value = 0.25, 75% of values between 0.15 and 0.3°). Its width was between 0.025 and 0.25° (median value = 0.05, 75% of values between 0.05 and 0.075°). Orientation was optimized to within 30° by measurement of an orientation-tuning curve. Three kind of stimuli were used: 1) the bar alone flashed in the center of the RF; 2) "surround-only" stimuli made of several bars identical to the center bar and flashed outside of the RF center, so they do not elicit any response; and 3) center/surround stimuli.
The bars were regularly spaced. The space between the central bar and the surround bars was increased until the elimination of any response to the surround-only stimuli. In some cases, however, the surround triggered neuron responses even when the bars were far away from the plotted RF. The space was then chosen to be sure that no bars of the surround encroached on the RF. One to three (typically 2, for 80% of the neurons) rings of surround bars constituted the surround stimulus. The surround stimulus was therefore made of 6, 18, or 36 bars. Typical stimuli with one ring of surround bars are shown on Figs. 7-9. The surround covered 1.4-7.9° of visual field. Typically, the surround diameter was 5-8 times (70% of the cases between 6 and 10 times) larger than the length of the bar and was 3-4° across (70% of the cases between 2.3 and 5.6°). Extreme values of 3-19 times the length of the bar were obtained for the largest and smallest VI RF.
The stimuli were named following Knierim and van Essen
(1992) and Nothdurft et al. (1999)
:
C, Center alone, bar flashed at the optimal orientation in the center of the RF of the neuron.
C/S, Center and iso-oriented surround (creating a uniform field of bars).
C/S', center and cross-oriented surround (creating an orientation contrast between the center and the surround).
C/l, Center and iso-oriented bars only along the axis of preferred orientation of the neuron (creating a discontinuous line of bars).
The "surround-only" stimuli were called, respectively S, S' and L.
The stimuli were presented for 500 ms with an inter-trial interval of 1 s, on a computer monitor driven by a Truevision Vista Board under the control of a Matlab program. Each recording run consisted of 20 repetitions of a set of the 7 stimuli interleaved in random order. At least three runs were carried out for each neuron.
V2 inactivation
We chose to use GABA injections for inactivation of V2
(Hupé et al. 1999). Inactivation by GABA has the
advantage of confining the inactivation zone to a limited region, which
was crucial given the proximity of areas V1 and V2. GABA inactivation
also spares the axons, which is important as the fibers coming from the
lateral geniculate nucleus (LGN) to V1 travel just along the deep
layers of V2. Finally, even large-scale GABA inactivation, when
properly done (Hupé et al. 1999
), has effects that
do not last too long, so it is possible to record V1 neurons after the
V2 inactivation to see functional recoveries from the effects. GABA
inactivation regions are always restricted (Hupé et al.
1999
): it was therefore not possible to inactivate the whole
area V2, as we had done in a previous study for MT using cryoloop
cooling probes (Hupé et al. 1998
). By using
several micropipettes filled with GABA, it was, however, possible to
inactivate a reasonably large portion of the region of V2 projecting
back to a given point of V1. To know where this point of V1 was, we
took advantage of the retinotopic laws of connections (McIlwain
1973
; Salin and Bullier 1995
): basically, neurons of different areas that look at the same point of the visual
space are interconnected.
Preliminary mappings were therefore done in V1 and V2 to find neurons in retinotopic correspondence. A microelectrode was inserted in V1 perpendicularly to the pial surface a few millimeters posterior to the lunate sulcus. A V2 site was chosen when the microelectrode hit the deep layers of V2 after traveling a few hundred micrometers through the white matter, remained in V2 for at least 1 mm and no more than 1.5 mm, then crossed the lunate sulcus (short period of silence) and reached an area with large RFs (V3 or V4; see Fig. 1A). We plotted on Fig. 1B the progression in RFs (dotted rectangles) obtained during a typical mapping penetration through V1, V2, and V3. In addition, but for monkey P only, the mapping microelectrode was removed and replaced by a device made of three microelectrodes spaced by about 2 mm from each other. This device served as a test device to determine the whole extent of the RF covered by the inactivation device. The plots obtained by these three electrodes are numbered (1, 2, and 3) in Fig. 1B. Another microelectrode was then placed in V1, several millimeters caudal and medial to the three-microelectrodes device, and penetrations were repeated until V1 RFs were found that were in the middle of the V2 RFs (1, 2, and 3). The chosen V1 site RF is represented by the filled black square on Fig. 1B. The V1 region in retinotopic correspondence with V2 was always several millimeters behind the V2 device, at least in our experimental conditions (the angle of the penetration in V1-V2 was adjusted to make it possible), so these neurons did not lie on the way of the inactivation device to V2, and therefore could be recorded in intact cortex.
|
The V2 mapping microelectrode (or the 3-microelectrodes device for monkey P) was then removed, and the dura matter was dissected to allow the penetration of a compound device made of six micropipettes filled with GABA 100 mM (monkeys N and P) or 200 mM (monkey Q) and three or five (monkey Q) recording microelectrodes (Fig. 1C). The V2 RF plotted for the microelectrode placed in the middle of the device (arrow 1 on Fig. 1C, E1 in Fig. 1D) is represented by the filled gray square on the Fig. 1B. The V1 and V2 RFs overlap. All the plotted V2 RFs belong to the region of V2 inactivated by GABA: this gives an idea of the aggregate of receptive fields (ARF) of the inactivated region. It is about 2.5° in diameter and very well centered on the V1 RF.
We used electrolytic lesions in V1 and V2 to aid reconstruction of electrode tracks on histological sections stained with cresyl violet. Figure 1A shows a photograph of a histological parasagittal section in V2 with a lesion (arrow) made at the end of the experiment by one of the microelectrodes of the device (7 µA for 7 s). We can see also the tracks of two elements of the device (probably 1 microelectrode and 1 micropipette) through the white matter and V2. Despite repeated GABA injections in V2, it is clear that the cortex remained in good condition until the animal was killed and perfused.
The device was built as previously described (Hupé et al.
1999). The micropipette tips were about 1 mm away from each
other; the microelectrodes were 350-700 µm away from one
micropipette, in the middle of and around the micropipettes (Fig.
1D). We designed the inactivation device so that the
microelectrode recordings could both give a good estimate of the size
and location of the V2 inactivated zone, and to check for the proper
inactivation of V2 neurons during the experiment. All the tips of the
micropipettes were always in one plane orthogonal to the long axis of
the micropipettes. The tips of the three microelectrodes were staggered
in depth, about 200 µm below, at the same level and about 700 µm
above the plane of the micropipette tips. This geometric disposition
along the main axis of the device can be seen on Fig. 1C,
with the tip of one microelectrode protruding in the middle of the
pipettes (arrow 1), and one microelectrode whose tip is
behind the other tips (arrow 2). We had shown previously
that, when injected in the cortex, GABA goes up along the pipettes
while diffusing, resulting in ellipsoid inactivation zones centered
well above the tip of the pipettes (Hupé et al.
1999
). We therefore wanted to place the tips of the
micropipettes in the upper third of V2 (i.e., in layer 3), so we could
inactivate both the superficial and the deep layers of V2, which both
send feedback connections to V1 (Barone et al. 1995
;
Kennedy and Bullier 1985
). The location of the
microelectrodes allowed us to check during the whole experiments that
the micropipettes were still in about the same position. These
microelectrodes allowed us also to check that GABA properly inactivated
both superficial and deep layers. The minimal extent of V2 region that
we consider to have fully inactivated is 2 mm wide (large black disk on
Fig. 1D). According to calculations based on the published
sizes of V2 RFs as a function of their eccentricity and on the V2
magnification factor (Gattass et al. 1981
), the ARF of a
2-mm-wide V2 region at 2.5° eccentricity should be about 3.5°: this
value fits quite well our own mappings made in situ and shown in Fig.
1B.
V2 inactivation was carried out by means of successive injection of 25 or 50 nl of GABA 100 or 200 mM simultaneously in the six pipettes
(Hupé et al. 1999). Recording of V1 neurons
started about 30 s after the first injection, to ensure that V2
was well inactivated when we started to test the effect of feedback
inactivation. These injections produced a complete inactivation of a V2
region 2-4 mm diam during the whole period of test (3.5 min) as
predicted by our preliminary experiments (Hupé et al.
1999
) and as verified by the microelectrodes placed at the
periphery of the inactivated region (Fig.
2).
|
GABA (100 or 200 mM) was dissolved in a solution of artificial cerebrospinal fluid (ACSF; in mM: 150 NaCl, 10 Glc, 1.2 NaH2PO4, 3 Kcl, 1.25 CaCl2, and 1 MgSO4, pH 7.2). The GABA solution was pumped by a Harvard PHD 2000 programmable pump that acted on six gas-tight 7110 Hamilton syringes (10 µl), connected to the glass capillaries of the device (A-M systems, 0.4 mm ID) with FEP tubing (CMA/Microdialysis) and corresponding tubing adaptors. The whole system was filled with the GABA solution and was free of bubbles. The device was positioned in V2 by gently lowering it through V1 and the white matter, avoiding surface blood vessels and continuously recording spike activity and ejecting GABA solution through the micropipettes to prevent intrusion of cortical material in the micropipettes and possible clogging. Volumes of GABA solution were injected according to computer-controlled protocols (Symphony software) with a precision of 2 nl.
Analysis of effects of V2 inactivation on the ON response strength
Spikes were counted between 5 ms before and 495 ms after
response onset. The method of latency measurement is described in the
accompanying paper (Hupé et al. 2001). The same
latency was used for all the stimuli and was the minimum one measured
for the stimuli C, C/S, C/S', and C/l. Note that the minimum latency was usually that of the response to the optimal stimulus, which was the
stimulus C in most of the cases. The mean spontaneous activity recorded
during each run was then subtracted.
We first compared for each stimulus the response strengths between two
control runs of 20 stimulus repetitions each (Hupé et al.
1998); if the test was significant, the response of the neuron
to this stimulus was discarded, and the response was considered as not
stationary. Sixty-six neurons were kept after this first stage of
analysis. Two of these neurons were not stationary for the stimulus C,
but were stationary for the stimuli C/S and C/S'; two other neurons
were not stationary only for the stimuli C/S or C/S'; 64 neurons were
therefore included for the analysis of the effects of V2 inactivation
onto the response to the stimulus C, and also 64 neurons were included
for the analysis of the orientation-dependent surround modulations, but
only 62 neurons were used in both studies. Tests were then done between
the control runs and the GABA run.
We used the bootstrap Student t-test (Efron and
Tibshirani 1993) with 10,000 bootstrap replications. As four
responses to different stimuli were studied simultaneously, there was
an increase of the type I error. The actual error was controlled with a
procedure adapted from Manly (1997)
: instead of applying
the same set of randomizations to the data, we applied the same set of
bootstrap replications. The significance level was here therefore a
controlled 5% type I error (see Hupé et al.
2001
).
We also tested the activity of the neurons when surround-only stimuli
were presented. The comparisons of such "responses" could be
statistically tricky, as most often there were only a few spikes, and
the "response" was irregular. The response histograms therefore not
only differed usually from the Normal distribution, but were also
asymmetric with a lot of zero values. We thus used the Randomization
test (Manly 1997) instead of the bootstrap
t-test if proportions of 0 values was larger than 2/3. The
logic was then not to compare the means any more, but to ask the
following question: is the number of times (that there are spikes when
the stimulus is present) different in control and when V2 is
inactivated? The three surround-only stimuli were compared
simultaneously with the usual procedure for multiple comparisons
(Manly 1997
).
Response categories
Cells were classified after the criteria of Nothdurft et
al. (1999), which were adapted from Knierim and van
Essen (1992)
. We were interested in two properties of the
surround: the orientation and the spatial distribution of the bars. We
computed two nonorthogonal sets of criteria. The labels for these two
sets (1st orientation, then spatial configuration) are indicated after
the name of the neuron within each box of Fig.
3.
|
SURROUND ORIENTATION COMPARISON SET (STIMULI C, C/S, AND C/S'). NM: Not Modulated cells. The mean responses to the stimuli C, C/S, and C/S' were not statistically different (1st 2 neurons of Fig. 3).
GS: General Suppression. C/S < C and C/S' < C (3rd and 4th neurons of Fig. 3). S: Suppression. C/S < C or C/S' < C, but not GS. OC: Orientation Contrast. C/S' > C/S (5th neuron of Fig. 3). UF: Uniform Field. C/S > C/S' (last neuron of Fig. 3). F: Facilitation (Enhancement). C/S > C or C/S' > C (last neuron of Fig. 3). All these categories are not mutually exclusive, and some neurons were therefore classified in two categories: for example the last neuron of Fig. 3 was a "UF" and a "F" neuron.SURROUND SPATIAL CONFIGURATION COMPARISON SET (STIMULI C, C/S, AND C/l). E-S: "End-Stopped." C/l < C. We used this term by analogy with the property of end-zone inhibition, even if we did not have the means to know whether these cells were really "end-stopped"1 (3rd, 4th, and 5th neurons of Fig. 3).
SI: Side Inhibition. C/l > C/S. The response was significantly suppressed by the flanks (or sides) of the surround (Bishop et al. 1973 ![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Effects of V2 inactivation on the ON responses of V1 neurons to a single bar flashed in the center of the RF
The responses of 6 of the 64 neurons decreased significantly during V2 inactivation. No increase was observed. We carefully checked the responses of these six neurons. We discarded the responses of three other neurons for which the change of response was also significant but very close to the 5% level, as we could not exclude definitively that the change might be due to poor stationarity.2 Note that 3/64 = 4.67% corresponds closely to the proportion of effects one would expect with a 5% error level. We excluded these neurons from this analysis (without deciding whether the effect was real or not) and therefore had 6 neurons whose response was significantly decreased over a population of 61 neurons. The mean responses to the single bar for these neurons are shown on Fig. 3 (left column within each box) during control (left column) and GABA (right column).
The time course of the effects of V2 inactivation on V1 responses is
illustrated in Fig. 4. Figure 4,
A and B, shows two examples of significant
decreases. The first example was one of the earliest responding neurons
in our sample, and the decrease was already significant
(P = 0.011) when the first 50 ms of response were compared in control and V2 inactivation conditions. The second example
was the neuron having the significant decrease that had the longest
latency; it showed no change for the first 50 ms of response
(P = 0.92). This example was the least representative of the sample, as can be concluded from looking at the population histogram in Fig. 4C. This histogram was computed the same
way as described in the previous paper (Hupé et al.
2001). The decrease of response is present from the beginning
of the response. Figure 4D shows the histogram of
differences of normalized responses, control minus GABA. Significant
differences can be observed after the first 20 ms of responses (2nd bin
of response). Given our small sample of affected neurons, it made no
sense to make multiple comparison procedure (MCP) tests (see
Hupé et al. 2001
). Significant results
(P < 0.05, 1-way test) of the classical Wilcoxon
(exact) tests are symbolized by the black line below the histogram.
|
Figure 5 presents the histogram of
latencies of the V1 neurons. As in the case of the MT inactivation
experiment (Hupé et al. 2001), even early
responding neurons in V1 could be affected by V2 inactivation.
|
Effects of V2 inactivation on the responses to the surround-only stimuli
We never observed any significant increase of the response to the three "surround-only" stimuli when V2 was inactivated, contrary to what we had observed in the preliminary experiments (see INTRODUCTION).
Analysis of the effects of V2 inactivation on center/surround interactions
ANALYSIS OF SINGLE NEURONS. We first looked at the responses of the V1 neurons for which the response to the stimulus C decreased during V2 inactivation (Fig. 3). The responses of these neurons to the center/surround stimuli also decreased, so the differences of response for the different stimuli, when present during control, were generally also present during GABA. We wanted to know whether these neurons share any common feature, especially with regard to the surround modulations. This was not the case because the neurons were homogeneously distributed in the different classes (Fig. 3, left boxes). All of these neurons were classified similarly for the orientation modulations during control and GABA (Fig. 3, right boxes), with the exception of one neuron that was UF (and F) during control and only F during GABA (note, however, that the classification test is less powerful in the GABA condition as there are less spikes). The modulations dependent on the spatial configurations seemed to be less stable: two neurons were not E-S any more, and one was not SI any more. However, it was not obvious when looking at the responses that there were major changes in these modulations.
We then looked for significant effects of V2 inactivation on the response to center/surround stimuli (C/S, C/S', and C/l). These effects were rare and rarely independent of the effect on the center-alone condition (not shown). The stimulus C condition was in fact the one for which we observed most often significant effects. However, this does not mean that there was no effect of V2 inactivation on the center/surround interactions, as the proper way of studying center/surround interactions is to compare simultaneously the changes of responses to the different stimuli: changes in the interactions could be present, whereas the response to each stimulus was not significantly affected. This happens when there is a modest increase of the response for one stimulus, and a modest decrease of the response for another stimulus. The interaction between the stimulus and the inactivation of V2 were thus studied for each neuron. Seventy neurons were studied with center/surround stimuli while V2 was inactivated with GABA injections. As we wanted to observe the possible effects of GABA on the interactions of response between all the stimuli, we did not reject at this stage of the analysis the responses that were significantly different between two controls for one of the stimuli. We looked at the interactions between the responses to the four center/surround stimuli and the effect of the treatment (control/GABA) with a (parametric) two-way ANOVA for each neuron. We also checked whether significant interactions were found when we did the test between the first and the second control. As long as only the global result of such an ANOVA matters, and not the post hoc comparisons, this test is robust even when the distributions are not Normal and the variances not always similar. For detailed comparisons, we had to use nonparametric tests (see METHODS). Ten neurons had been tested with only one control, and had no interaction effect [F(3,x), P > 0.05]. Sixty neurons were tested first with a two-way ANOVA between the four stimulus conditions and the three runs (2 controls and 1 GABA). If the interaction was significant, these neurons were also tested with two other two-way ANOVAs, between the two controls, and between the mean control and the GABA. Fifty-five neurons had no significant interaction [F(6,x), P > 0.05]. Five neurons had an interaction effect [F(6,x), P < 0.05]; two of them had a significant interaction effect between the two controls, two between the average control responses and the responses during V2 inactivation, and one was significant for both tests. In conclusion, if one just addresses the question of the effect of V2 inactivation onto the surround modulations in V1, 3/70 = 4.3% neurons were significantly affected, given a type I error of 5%. This proportion of observed effects matches very well the expected 5% error level. About the same proportion of effects was observed when the test was done between the two controls: 3/60 = 5% of the neurons showed a significant P value, whereas nothing had been changed between these two conditions (false-positive cases). One can conclude therefore that these effects of V2 inactivation might be due to chance. However, this analysis could have missed some influences of V2 inactivation too small to reach the significance level in individual neurons, but that could appear at the level of the population. In addition, the analysis averaged the whole response during 500 ms and could therefore have missed effects in the temporal domain. We therefore carried out a population analysis to increase the signal/noise ratio.POPULATION ANALYSIS.
To pool together the responses of different neurons, we first had to
identify subpopulations of neurons homogenous for the type of surround
modulations (see METHODS). The breakdown of the population
(64 neurons) in the different classes of the surround orientation
comparison set is presented in the pie-chart of Fig. 6. Our proportions of GS (33%), OC
(19%), and UF cells (6%) are smaller than those described by
Nothdurft et al. (1999), as expected given the fact that
our criteria are more conservative. The differences between their and
our proportions were, however, not statistically significant.3
|
|
|
|
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Inactivation
It is always difficult to assess the validity of negative results: the conviction that center/surround interactions of V1 neurons do not depend on feedback from V2 depends therefore on the efficiency of our inactivation method.
INACTIVATION OF NEURONS WITH GABA.
GABA has been used in numerous studies to inactivate neurons, and we
had also made extensive tests of this method
(Hupé et al. 1999). The validity of V2
inactivation was also assessed by recording with microelectrodes in V2
that were attached to the injection micropipettes. However, some
micropipettes were far away from any microelectrode, and we could not
control physiologically the effects of GABA injections in these
pipettes (see Fig. 1D). Clogging of some of the
micropipettes during the experiment might therefore have happened,
although the openings of the pipettes were large: 30-35 µm OD,
15-20 µm ID with an additional bevel of 30-40 µm
(Hupé et al. 1999
). In addition, the
setup was designed in order that any clogging during the experiment
would be detected rapidly: all junctions from the syringes to the
micropipettes were tight, and the type of syringes as well as the way
of filling-in the micropipettes with GABA allowed us to be sure that
there were no air bubbles in the whole injection line. No compression
was possible, and the only way out for GABA was the tip of the
micropipettes. We had tested the setup with clogged micropipettes and
observed that in this case the tubing adaptor slipped along the needle of the syringe until the tubing disconnected from the syringe. This
happened after a few hundreds of nanoliters of GABA injection. This
never happened during the three experiments described here; we also
checked that there was no visible slipping of any of the tubing adaptors.
INACTIVATION OF THE CONVERGENCE ZONE FROM V2 TO V1.
Anatomical studies could give us an idea of the spatial extent of the
V2 neurons that project to a given point in V1 (the convergence zone of
Salin et al. 1992). Typically, after 0.5- to 1-mm wide
injections of Cholera Toxin B in V1, the maximal extent of retrograde
label in layers 5/6 was 3-6 mm along the antero-posterior axis (i.e.,
across the V2 CO stripes), and 7-9 mm along the medio-lateral axis
(i.e., along the CO stripes) (A. Angelucci, personal communication).
TOTAL INACTIVATION OF AN INPUT IS NOT A PRIORI NECESSARY FOR
OBSERVING FUNCTIONAL EFFECTS OF THE INACTIVATION.
Other studies have shown the function of cortical connections by
inactivating only a part of them (Alonso et al. 1993;
Martinez-Conde et al. 1999
; Merabet et al.
1998
). This is particularly evident for the studies of
intrinsic long-range connections, which have been studied by Crook and
co-workers (Crook and Eysel 1992
; Crook et al.
1996
, 1998
) with GABA inactivation, which were
at least one order of magnitude smaller than ours. In addition, we had a functional proof of the efficiency of V2 inactivation, as significant decreases on the responses of V1 neurons to a single bar were observed.
V1 WAS NOT INACTIVATED BY GABA.
As we observed effects on the V1 responses, this is an important point
to address. We are confident on this point because the white matter
between V1 and V2 acts as a barrier for GABA diffusion, as directly
tested previously (Hupé et al. 1999). Also, we never saw a general decrease of the response in V1 when we
reached the deep layers.
Effects of V2 inactivation on the responses of V1 neurons
The responses to the bar flashed in the center of the RF decreased
when their feedback input from V2 was inactivated in 10% (6/61) of our
sample. This was quite unexpected, as it is usually assumed that the RF
properties of V1 neurons are shaped by both their LGN input and
intrinsic connections within V1, the debate being rather of the
relative weight of the feed-forward and intrinsic influences
(Sompolinsky and Shapley 1997). This result is, however, in good agreement with the study of feedback connections from MT: we
had found that the responses of V1, V2, and V3 neurons to a single
moving bar were affected in 40% of the sample when MT was inactivated
(Hupé et al. 1998
).
All the effects observed in V1 with V2 inactivation were observed in
only two penetrations, and four of them were observed in a single one.
It could be argued that the inactivation method was efficient only for
these two penetrations, where the proportions of affected neurons were
4/11 and 2/13, i.e., 36 and 18% of the neurons. The first value gives
a proportion similar to what had been observed for the V1, V2, and V3
neurons when area MT was thoroughly inactivated (Hupé et
al. 1998).
An alternative explanation could be that the role of V2 feedback
connections depends crucially on some specific properties of V1
neurons. As neurons that share the same properties are often clustered
(DeAngelis et al. 1999; Maffei and Fiorentini
1977
; Payne et al. 1981
), this would explain why
we found effects in some penetrations and not in others. Because we did
not analyze all the properties of V1 neurons, we could not really test
this hypothesis. We did not find any specificity of the affected
neurons concerning the size of the RF or the orientation selectivity. The affected neurons were also distributed in both superficial (3 neurons) and deep layers (3 neurons). This small sample precluded any
conclusion concerning the general properties of the V1 neurons affected
by V2 inactivation.
Interestingly enough, all the effects consisted in decreases of the
responses, confirming the predominantly excitatory influence of
feedback connections that we had found when MT was inactivated: 84% of
the effects for the bar moving alone were decreases of response
(Hupé et al. 1998). This excitatory influence is
also in agreement with the results found in the rat (Gonchar and
Burkhalter 1999
; Johnson and Burkhalter 1996
,
1997
; Shao and Burkhalter 1996
). These
findings contradict the results of Sandell and Schiller (1982)
, who found increases as well as decreases of V1
responses when they inactivated area V2 of the squirrel monkey. This
discrepancy can be either due to the species that they used, or to the
lack of control of their inactivation method, as they did not check whether some V1 cells were not directly inactivated by cooling, as
already noted by Salin and Bullier (1995)
, or even to
different statistical techniques.
Even if we did not study whether the effects of V2 inactivation depended on the parameters of the center bar (we did not measure orientation curves during GABA injections, for example), it seems, however, that the excitatory influence from V2 is rather nonspecific, as when the response to the bar was decreased, similar decreases of response were observed for the center/surround stimuli, or even for the surround-only stimuli in the cases where it was present (see the 2nd and 6th examples of Fig. 3). The response gain of some V1 neurons could therefore be controlled by the feedback from V2.
In the preceding paper we showed that the effects of feedback
connections onto V1-V3 are extremely rapid. However, this may be
related to the fact that MT neurons are activated early after visual
stimulation, possibly by connections bypassing area V1 (see
DISCUSSION of the preceding paper). It was therefore
interesting to study another model of feedback for which there is no
such limitations. Feedback connections from V2 to V1 are interesting because, even if there are some direct connections from the LGN to V2
(Bullier and Kennedy 1983), which therefore bypass V1,
this pathway does not seem to be functionally autonomous, as
inactivation of V1 leads to a complete silence of V2 neurons
(Girard and Bullier 1989
; Schiller and Malpeli
1977
). Second, V2 neuron responses lag V1 responses by about 10 ms (Nowak et al. 1995
), and most sharp cross-correlogram
peaks are displaced from the origin in a direction compatible with a
drive from V1 to V2 (Nowak et al. 1999
; Roe and
Ts'o 1999
). We therefore expected that feedback influences
from V2 to V1 would be delayed, as is usually assumed for feedback
connections in general (Knierim and van Essen 1992
; Lamme et al. 1998
). Contrary to our hypothesis, but
similarly to the result of the inactivation of feedback connections
from MT, there was no visible delay of the effects of V2 inactivation on the responses of V1 neurons. The decrease of response when the
feedback input was removed was visible in the first 20-ms bin of
response and significant after 20 ms. Early effects were observed in
neurons with short latencies as in the experiment with MT inactivation
(Hupé et al. 2001
). In another sample recorded in
preliminary experiments described earlier (Bullier et al.
1996
), we also found decreases of the response to stimulation
of the RF center when V2 was inactivated. These decreases were also
observed most often at the onset of the response (see Fig. 1 of
Bullier et al. 1996
).
Given the fact that the latencies of the responses of V2 neurons lag V1
latencies by about 10 ms, it was quite surprising that influences of
feedback connections could be observed within the same order of
temporal magnitude. Note, however, that the conduction times between V1
and V2 can be very short (about 1 ms: Girard et al. 2000), and that a
delay of up to about 15 ms for one fast V1-V2-V1 loop could go
undetected given our temporal resolution.
The rapid feedback effects on V1 neurons after V2 inactivation suggests
that what we observed in the case of MT inactivation (Hupé
et al. 2001) was not due to the specific temporal properties of
this area but that it is a general property of feedback connections that usually act on the entire temporal extent of the response. This
makes sense if we recall that the initial part of the response of a
neuron carries 70% of the information (Heller et al.
1995
; Tovee et al. 1993
). Acting on the initial
part of the response is therefore essential if feedback connections
play a role in the processing of visual information by the cortex.
Absence of effects of V2 inactivation on the center/surround interactions in V1 neurons
Contrary to what we expected, we could not detect any modification of the center/surround interactions in V1 neurons when V2 was inactivated. Even if we were not sure of inactivating the whole convergence zone of V2 to V1, the proportion of the inactivated region was sufficiently large that we could expect to see at least some change in the responses to the center/surround stimuli. The effects on the center response were conclusive in that respect. The fact that these neurons kept their surround modulations whereas their general level of activity changed (Fig. 3) is a strong argument in favor of mechanisms responsible for the center/surround modulations that do not depend on the V2 feedback. Moreover, we tested numerous V1 neurons located in the tracks where effects had been observed on the center response, the V2 inactivation being done then exactly in the same conditions, and the overlap of the RF being also identical, and no effect was observed on the center/surround interactions.
Comparison with previous studies
In previous experiments made on four other monkeys, we had
recorded more than 100 neurons. We used three micropipettes of GABA 100 mM, creating inactivation zones larger than those reported in other
studies where a single micropipette was often used (Alonso et
al. 1993; Crook et al. 1998
;
Martinez-Conde et al. 1999
; Merabet et al.
1998
). Even if we know that inactivation of such a size could
not a priori inactivate all the V2 neurons of a convergent zone, it is
likely that at least in some of these experiments we inactivated a
great part of the V2 feedback input of the V1 tested neurons. In these
experiments also, we never saw any specific change of the
center/surround modulations. As mentioned above, we had observed in a
few cases decreases of the response for the bar flashed in isolation in
the center of the RF (Bullier et al. 1996
), and we
reproduced this result in the present experiments.
On the contrary, we were not able to replicate in the present
experiments our earlier finding of increases to responses of surround-only stimuli (Bullier et al. 1996). This can be
verified on the population histograms presented in RESULTS,
where the responses to the surround only stimuli are always plotted.
Even neurons that gave a little response to these surround-only stimuli
showed no increase of response. A possible explanation for the
discrepancy of the results of both studies could be that the
surround-only effects would have been precisely due to a partial
inactivation of V2 (leading to an asymmetry of the feedback
influences). A more likely explanation is that the surround-only
effects reported earlier could have been due to an increase of the size
of the RF concomitant to a change of the EEG
state.4
We have several arguments in favor of this explanation. First of all,
when looking back at some neurons whose response had been only recorded
in control condition but not subjected to a test of V2 inactivation
because of poor stationarity, we could observe indeed that a response
to the surround-only stimulus was present in one of the two controls.
Second, we measured the EEG activity of the three monkeys for which the
results have been presented here, and we did observe large increases of
surround-only responses in control runs, increases that were correlated
to increases of synchronization of the EEG, in perfect agreement with
the results of Wörgötter et al. (1998). Even
if we cannot rule out that our previously observed effects of V2
inactivation could have some link with the role of feedback connection
(different causes being able to produce similar effects), it is,
however, more likely that they were due to changes in the general EEG state.
In our last three experiments, not only could we better assess the level of anesthesia by on-line checking of the EEG, but also all the recordings were checked off-line. When a change in the EEG power could be observed between controls and GABA, the neuron was rejected for further analysis. The 70 neurons kept for analysis and presented in this paper were all the neurons that successfully passed this initial step.
Neurophysiological basis of center/surround interactions
CENTER/SURROUND INTERACTIONS WITH STIMULI MADE OF BARS OF DIFFERENT
ORIENTATION OR DISPOSITION.
The effect of the surround most often observed in control condition was
a strong suppression of the response irrespective of the orientation
and spatial parameters, agreeing with what has been observed in other
studies made on the macaque monkey (Knierim and van Essen
1992; Nothdurft et al. 1999
). As noted by those
authors, the nonspecific suppression arising homogeneously from
stimulation of the surround is a general property of neurons found at
all levels of the visual system, starting with retinal ganglion cells.
General suppression might therefore be transmitted and amplified from
low to higher levels through feed-forward projections. This hypothesis
is supported by the observation that general suppression is always
observed from the beginning of the response (Fig. 7) (see also
Knierim and van Essen 1992
; Li et al.
2000
; Nothdurft et al. 1999
), and that the near
surround is the most powerful region to inhibit the responses to
stimulation of the RF center (Born and Tootell 1991
;
Li et al. 2000
; Nothdurft et al. 1999
).
NEAR VERSUS FAR SURROUND INFLUENCES.
Our stimuli contained a smaller number of bars (6-36, typically 18)
than the stimuli used in previous studies and covered therefore a
smaller region of the visual field (typically 3-4°, see
METHODS) than in these studies where the entire screen was covered by the stimulus (Knierim and van Essen 1992;
Nothdurft et al. 1999
). The modulations of the center
response are, however, maximal near (<2°) the border of the RF
(Born and Tootell 1991
; Li et al. 2000
;
Nothdurft et al. 1999
). The amplitude of our modulations was indeed comparable to what was observed by Knierim and van Essen (1992)
in the awake monkey and Nothdurft et al.
(1999)
in the anesthetized monkey.
OTHER SURROUND PROPERTIES.
Many center/surround properties are present in V1 neurons (Li
and Li 1994). It is not impossible that surround modulations other than the ones we have studied depend on feedback from V2. Results
from an earlier study (Hupé et al. 1998
)
suggest that this is likely. We tested the role of feedback connections
from MT onto the responses of V1, V2, and V3 neurons. We used moving stimuli of the figure/ground type, so direct comparisons cannot be done
with this study. However, the suppressions induced by the moving
background are akin to the surround suppression obtained with flashed
stimuli. When the neurons were tested at high salience (high luminance
bar over a low contrast background) and MT was inactivated by cooling,
the background suppression of V1 and V3 neurons were still present and
as strong as during the control period (Bullier et al.
2000
; Hupé et al. 1998
). But
when low salience stimuli were used, the strong suppression by the
moving background almost disappeared when MT was inactivated
(Bullier et al. 2000
; Hupé et al.
1998
). The results obtained at high salience are comparable to
those obtained in the present study: when a background stimulus
modulates the response to a high contrast bar, inactivating the
feedback connections produces no effect on this modulation. The effects
observed at low salience may be specific for the feedback from MT,
which is specialized for processing low contrast moving stimuli. This
positive result suggests that some center/surround interactions that
reflect specific properties of area V2 could be shown to be dependent
on the feedback from V2.
ROLE OF FEEDBACK CONNECTIONS FROM V2 TO V1.
We conclude that feedback connections from area V2 do not play a
role in the center/surround interactions observed in V1 neurons, at
least those generated with the present set of stimuli in the near
surround and with variable orientation and spatial disposition of
distributed bars. This negative result is important, since these
interactions have been extensively studied, and since the temporal
delay of their involvement had led several authors to suspect the role
of feedback connections from V2. The surround orientation contrast
property is supposed to play a role in pop-out properties,
which are supposed to be due to a preattentive treatment of visual
information. Such preattentive treatments have been described as
bottom-up (Wolfe 1994). Our results suggest
therefore that feedback connections are not involved in such a
bottom-up treatment of information. As mentioned above, it is still
possible that some center/surround interactions specific to the
properties of V2 neurons will be shown to depend on feedback connections.
![]() |
APPENDIX |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Facilitation
Six neurons were classified F and not OC nor UF. This proportion
is greater than the proportion found by Nothdurft et al. (1999), but these neurons presented also a small response to
the surrounds presented in isolation, which could explain the response to the C/S and C/S' condition almost by a linear summation. The timing
of the facilitation corresponded to the latency of the surround-only
condition (facilitation observed in the 2nd bin of response, 20-40
ms). No effect of V2 inactivation was observed on these neurons (see
Fig. A1, A and
B).
|
Uniform field
Only four neurons were found in this category. It seemed that the orientation-dependent modulation was delayed. There was a strong transient response to the surround-only stimuli, which interestingly enough was not orientation selective, and could not therefore explain the orientation-specific surround modulation by a linear mechanism. Both phasic responses to C/S and C/S' were even a little smaller than the response to the bar alone (see Fig. A1, C and D).
Not modulated cells
Twenty neurons showed no statistically significant modulation when tests were done on the whole response. However, it appeared that in the average there was a nonorientation-specific suppression of the early response (see Fig. A2A). This suppression seemed to decrease during V2 inactivation (Fig. A2B). To address the question of a possible effect on the early modulations of the response, we computed the response over the first 100 ms of response and made the classification again. Over the 20 NM neurons, 6 had a significant early surround suppression (Fig. A2C). GABA injections in V2 had, however, no effect on this modulation (Fig. A2D).
|
We also computed the late part of the responses, from 100 to 500 ms, and made the classification tests again. We specifically looked at the significant late enhancements of response. Then we selected the neurons for which the early response (0-100 ms) was not modulated by the surround (precisely the early response did not increase more than 5% if ever it increased for the given surround). Thirteen neurons matched these criteria. No effect of V2 inactivation was found on this late modulation (Fig. A2, E and F).
End-stopped cells
The modulations of the iso-oriented surround (S) were compared with the modulations originating from the regions aligned with the axis of preferred orientation of the neurons (stimulus L, for "line").
For the 15 neurons classified End-Stopped in the control condition, the response to the whole surround C/S was also always significantly suppressed. The suppression originated from the beginning of the response, as for the GS, and there was no effect of V2 inactivation. Ten of 15 neurons were still significantly E-S during V2 inactivation. Among the five neurons not significantly E-S anymore during the GABA injection, only one of them had been significantly E-S for both controls. On the other hand, one neuron was classified E-S only during V2 inactivation. Population PSTHs were simular during the control and when V2 was inactivated (not shown).
To target the neurons for which the suppression originated
predominantly from the end-zones of the RF, we selected the neurons for
which at least 70% of the total inhibition obtained for C/S was
already present with the stimulus C/l, i.e., C/l < C 0.7*(C
C/S). Seven neurons fulfilled this requirement; the
population PSTHs obtained this way were very similar to the previous
ones, and no effect of V2 inactivation could be observed (not shown).
Thirty-six neurons were neither E-S nor SI; the population histograms showed superimposed traces for the response to stimuli C and C/l both in control and GABA conditions (not shown).
![]() |
ACKNOWLEDGMENTS |
---|
We thank A. Angelucci for comments on the manuscript. We also thank N. Chounlamountri for help with the histology and G. Clain for the care of the animals.
This work was supported by Biomed Grant BMH4-CT96-1461.
Present address of A. C. James, P. Girard, and J. Bullier: Centre de Recherche Cerveau et Cognition, Centre National de la Recherche Scientifique-Université Paul Sabatier U5549, 133 route de Narbonne, 31062 Toulouse Cedex, France.
![]() |
FOOTNOTES |
---|
1 We did not measure the response of the neuron to a single bar of increased length.
2 The response changed already between the two controls, not significantly, but with the same trend as the observed change during V2 inactivation. Moreover, the responses did not recover, and it was not possible to decide whether it was due or not to a partial recovery of V2. These three neurons were, however, kept in the analysis of center/surround interactions.
3
It should be stressed that it is quite
unrealistic to give a precise idea of the percentage of neurons
belonging to the different categories. In addition to the fact that
neurons can change of modulation type with changes in the parameter of
stimulation (Li and Li 1994), it should be stressed that
neurons showing the same surround modulations were usually clustered,
as it is the case for most neurons properties. The final distribution
of neurons between the different categories would at the end depend on
the explored territories. The study of several neurons belonging to the
same class can just hopefully help us to increase the signal-to-noise ratio, to make more precise conclusions concerning the behavior of
single cells.
4
The fact that a perfect recovery of the initial
response occurred in some instances, which we presented
(Hupé et al. 1997) and published (Bullier
et al. 1996
; Payne et al. 1996
), seemed to reach
the limits of the probability: it appears unlikely that the change in
EEG occurred precisely during the period of V2 inactivation and not
during other periods. However, responses to stimuli activating only the
surround were not observed to change during the control period because
such cases were rejected from our sample because of poor stationarity
or because we judged that the stimulus was too close to the RF center.
Concerning the recovery period, we were not surprised by responses
during recovery that differed from the control or the GABA period
because we knew from earlier experiments that the total recoveries of
all the neurons after GABA injections could take up to 1 h
(Hupé et al. 1999
), and rebounds of activity in V2
could a priori produce strange effects. Thus we did not test for the
presence of changes in response to surround-only stimuli either between
the controls or between the GABA and recovery runs and we analyzed
only the changes that occurred during the V2
inactivation. Such changes could have occurred a lot more frequently,
explaining that sometimes we could observe them during the V2
inactivation period.
Present address and address for reprint requests: J.-M. Hupé, Center for Neural Science, New York University, 4 Washington Place, New York, NY 10003 (E-mail: hupe{at}cns.nyu.edu).
Received 20 March 2000; accepted in final form 6 September 2000.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|