Download The cortical visual area V6: brain location and visual topography

European Journal of Neuroscience, Vol. 11, pp. 3922±3936, 1999
Ó European Neuroscience Association
The cortical visual area V6: brain location and visual
topography
Claudio Galletti, Patrizia Fattori, Michela Gamberini and Dieter F. Kutz1
Dipartimento di Fisiologia umana e generale, Universita¢ di Bologna, Piazza di Porta S. Donato 2, 40127 Bologna, Italy
1
Department of Zoology and Neurobiology, Ruhr-University Bochum, D-44780 Bochum, Germany
Keywords: macaque monkey, parieto-occipital cortex, superior parietal lobule, visual topography, visuomotor integration
Abstract
The brain location and topographical organization of the cortical visual area V6 was studied in ®ve hemispheres of four awake macaque
monkeys. Area V6 is located in the caudal aspect of the superior parietal lobule (SPL). It occupies a `C'-shaped belt of cortex whose
upper branch is in the depth of the parieto-occipital sulcus (POS) and lower one is in the depth of the medial parieto-occipital sulcus
(POM), with the medial surface of the brain as a zone of junction between the two branches. Area V6 contains a topographically
organized representation of the contralateral visual ®eld up to an eccentricity of at least 80 °. The lower visual ®eld representation is
located dorsally, in the ventral part of POS, and the upper ®eld ventrally, in the dorsal wall of POM. The representation of the horizontal
meridian forms the posterior border of V6. It is adjacent to area V3 in POS as well as in the caudal part of POM, on the ventral convexity
of the brain. The lower vertical meridian forms the anterior border of V6, adjacent to area V6A. The upper vertical meridian is in the depth
of POM. The representation of the central visual ®eld is not magni®ed relative to that of the periphery. The central visual ®eld (below 20±
30 ° of eccentricity) is represented in the medial-most aspect of the annectant gyrus, in the lateral part of the posterior bank of POS. The
visuotopic organization of area V6 suggests a role in the analysis of the ¯ow ®eld resulting from self-motion, in selecting targets during
visual searching as well as in the control of arm-reaching movements towards non-foveated targets.
Introduction
The prestriate cortex of primates contains many representations of the
visual ®eld, each one of them considered as a different functional
area. Some of these representations show a point-to-point retinotopic
organization, while others a cruder visual topography. In the macaque
for instance, areas V2 and V3 represent a large part of the visual ®eld
in a highly orderly manner (Van Essen & Zeki, 1978; Gattass et al.,
1981, 1988; Burkhalter et al., 1986), while areas V3A, V4 and V5
show a coarser topographic organization (Van Essen & Zeki, 1978;
Gattass & Gross, 1981; Van Essen et al., 1981; Gattass et al., 1985,
1988).
Quite recently, a further representation of the visual ®eld was
discovered in the prestriate cortex located in the precuneate gyrus of
the macaque brain. It was called the parieto-occipital area (PO, Covey
et al., 1982). Area PO was reported to occupy the anterior bank of the
parieto-occipital sulcus (POS), and to extend onto adjacent portions
of the medial surface of the hemisphere medially and the medial bank
of the intraparietal sulcus (IPS) laterally. It contained a complete
representation of the contralateral visual ®eld, although the visual
®eld appeared to be discontinuously represented within the area
(Gattass et al., 1985). The central 30 ° of the retina was represented in
three different parts of PO, two dorsally and one ventrally, so that
Gattass and co-workers advanced the hypothesis that what they had
called area PO `may be more than one visual area' (see Gattass et al.,
1985, p. 9). Actually, the same authors found that the cells of the
dorsal zone of PO gave consistently weaker visual responses with
Correspondence: Professor C. Galletti, as above.
E-mail: [email protected]
Received 9 December 1998, revised 7 May 1999, accepted 9 July 1999
respect to those in the ventral one. In addition, it was reported that the
dorsal zone had a set of connections different from that found for the
ventral one (Colby et al., 1988). The term PO was then retained to
indicate the ventral, visually more responsive region of the originally
described area PO, leaving unnamed the visually less-responsive
cortical region dorsal to it (see Colby et al., 1988).
The functional characteristics of cells in the precuneate cortex of
the macaque brain have been recently studied in awake animals
(Galletti et al., 1991, 1996, 1999). Two functional areas have been
found there: area V6A, containing visual neurons as well as neurons
insensitive to visual stimulation; and area V6, whose cells are all
responsive to visual stimulations. Area V6A is a horseshoe-like strip
of cortex that occupies the dorsal region of the anterior bank of POS,
and extends onto adjacent portions of the medial surface of the
hemisphere medially and the medial bank of IPS laterally (Galletti
et al., 1999). Area V6 is located ventrally and posteriorly with respect
to V6A in the deepest part of the anterior bank of POS (Galletti et al.,
1996). It is likely that area V6 corresponds to area PO, according to
its last de®nition (Colby et al., 1988), while area V6A corresponds to
the weakly responsive region dorsal to it, though some inconsistencies have been observed (see Galletti et al., 1996).
The aim of the present work is to describe the brain location,
extent, limits and visual topography of area V6. Preliminary data on
this matter have been previously published in abstract form (Galletti
et al., 1998).
Materials and methods
Experiments were carried out on four monkeys (Macaca fascicularis;
3.1±7.1 kg) trained to perform a visual ®xation task. Experimental
Visuotopic organization of area V6 3923
FIG. 1. Microelectrode penetrations through the cortex of POS. (A and B) Two parasagittal sections of the brain of case 16R, taken at the level shown on the dorsal
view of the brain reported at the centre of the ®gure. Letters `a', `b', `c' and `d' on the sections indicate the reconstructions of four microelectrode penetrations
passing through the occipital pole and reaching the cortex of POS in the depth. Dashed lines on the grey matter mark the limits between different cortical visual
areas. In the bottom part of the ®gure, the reconstructions of RF sequences encountered along these penetrations are reported. In some cases, a continuous line joins
the RF centres of cells recorded from the same area. The numbers along these lines indicate the ®rst and last RF encountered along each cortical area. V1, V2, V3,
V6, V6A, areas V1, V2, V3, V6 and V6A; CAL, calcarine ®ssure; CIN, cingulate sulcus; IPL, inferior parietal lobule; IPS, intraparietal sulcus; LS, lunate sulcus;
POM, medial parieto-occipital sulcus; POS, parieto-occipital sulcus; SPL, superior parietal lobule.
protocols were approved by the Bioethical Committee of the
University of Bologna, and were complied with the National and
European laws on the care and use of laboratory animals. Detailed
descriptions of training, surgical and recording procedures, as well as
visual stimulation, anatomical reconstruction of recording sites and
animal care are reported elsewhere (Galletti et al., 1995). The
following is a brief description of them.
Animals sat in a primate chair facing a large (80 3 80 °) tangent
screen. They performed a ®xation task with the head restrained while
single neurons from the cortex of the precuneate gyrus were
extracellularly recorded by glass-coated Elgiloy microelectrodes
(Suzuki & Azuma, 1976). Eye positions were recorded using an
infrared oculometer (Dr Bouis, Germany; Bach et al., 1983). The
sample rate for action potentials was 1 kHz and that for eye position
100 Hz.
Once a single cell was isolated, its visual receptive ®eld (RF) was
mapped by using visual stimuli of different form, colour, size,
orientation, direction and speed of movement, rear-projected on the
screen facing the animal. Occasionally, also the RFs of small clusters
of cells were mapped. RF mapping started by oscillating the optimal
stimulus at successive points away from the centre of the visually
responsive region until the cell no longer responded. The screen
locations where the response was lost were marked as RF edges. The
locations of these edges were then con®rmed, and if the case
modi®ed, by entering with the appropriate visual stimulus into the RF
from outside, with the correct orientation, direction and speed of
movement (many V6 neurons were direction and orientation selective
and were sensitive to particular speeds of movement; see Galletti
et al., 1996). RFs were drawn as squares or rectangles parallel to the
axis of best orientation. RF sizes and locations were then transferred
to a database together with the other functional characteristics of the
studied cells.
At the end of the recording sessions, the electrode tracks and the
approximate location of each recording site were reconstructed on
parasagittal sections of the brain on the basis of marking lesions and
several other cues, e.g. the coordinates of penetrations within the
recording chamber, the kind of cortical areas passed through, the
location of boundaries between white and grey matter, and the
distance of recording site from the surface of the hemisphere.
Because our penetrations often reached very deep and convoluted
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
3924 C. Galletti et al.
FIG. 3. RF size versus eccentricity in prestriate areas. Regression plots of RF
size (square root of area) against eccentricity in degrees (°e) for cells recorded
in areas V2 (n = 485), V3 (n = 353), V6 (n = 466) and V6A (n = 408). The
regression equations are as follows. Area V2: size = 1.2 ° + 0.12 °e; r2 = 0.63.
Area V3: size = 3.6 ° + 0.19 °e; r2 = 0.55. Area V6: size = 4.8 ° + 0.43 °e;
r2 = 0.45. Area V6A: size = 21.3 ° + 0.21 °e; r2 = 0.14.
FIG. 2. RF size versus eccentricity in area V6. (A) Regression plot of RF size
(square root of area) against eccentricity in degrees (°e) for 466 cells recorded
in area V6. The regression equation is: size = 4.8 ° + 0.43 °e; r2 = 0.45. (B) Dual
regression plot of RF size against eccentricity for V6 cells with RF in the
upper (®lled circles) and lower (empty circles) visual ®eld (VF), respectively.
The regression equations are as follows. Upper VF (n = 91): size = 10.2 ° + 0.43 °e; r2 = 0.31. Lower VF (n = 375): size = 4.5 ° + 0.40 °e;
r2 = 0.49. ANCOVA analysis established that the two regression lines were not
signi®cantly different in slope (F1,462 = 0.1905; P > 0.6), but they were
signi®cantly different in elevation (mean difference in RF size = 6.8 °;
F1,463 = 93.6; P < 0.0001).
cortical regions, straight and sturdy electrodes were used to minimize
electrode bending during penetrations, and particular attention was
paid in reconstructing penetrations lacking in marking lesions.
Several cross-controls were carried out between the above-mentioned
criteria, so that the ®nal position of penetrations on brain sections was
that which matched the highest number of these criteria.
FIG. 4. Visual ®eld representation in V6. The ®lled circles indicate the
retinotopic distribution of RF centres of the same cell population shown in
Fig. 2. An outline of the most peripheral RF borders is also reported.
Results
General remarks
A total of 226 microelectrode penetrations were carried out in ®ve
hemispheres of four awake, behaving animals. Penetrations were
usually made in each hemisphere in a grid pattern with spacing of
1 mm. In some cortical regions a ®ner grid was used. Microelectrodes
entered through the dura mater and the cortex of the dorso-medial
part of the occipital pole along a parasagittal plane; they were tilted
30±40 ° with respect to a coronal plane.
As shown in Fig. 1, penetrations could reach deep into both banks
of POS. All cells encountered in the posterior bank of POS were
responsive to visual stimulation. They were assigned to areas V2, V3
or V6 on the basis of the pattern of RF location sequences observed
along the penetration. Cells were assigned to areas V2 or V3 when
their RF locations and sequences agreed with the well-known visual
topography of these cortical areas (see Gattass et al., 1981, 1988).
They were assigned to area V6 when the sequence of RF locations
followed the typical pattern of V6, that will be described later on in
this section.
Cells recorded from the anterior bank of POS were either visual or
non-visual in nature, and were assigned to areas V6 or V6A according
to the functional criteria described in Galletti et al. (1996). Note that
one of these criteria was the different pattern in the sequence of RF
locations observed along a penetration. This different pattern between
V6 and V6A is visible in penetrations `a' and `c' in Fig. 1. While in
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
Visuotopic organization of area V6 3925
FIG. 5. Brain location, extent and limits of area V6 in case 16R. (A±E) Parasagittal sections of the brain taken at the levels shown on the brain silhouette reported
on the top left of the ®gure. Shaded areas on each section indicate the extent of V6 at that parasagittal level. Arrowheads in (D,E) indicate the two branches of POS.
Other details and abbreviations as in Fig. 1.
area V6 the RFs `move' coherently along the penetration, in a certain
direction and with a physiological scatter (penetration `a'), in area
V6A they often jump in different directions, so that cells near one
another in the cortex can have RFs in completely different locations
in the visual ®eld (penetration `c'; see also Galletti et al., 1999).
Another distinctive feature among the cells of areas V2, V3,
V6 and the visual cells of V6A was the size of their RFs. We
have constantly observed that in area V6 the RFs were larger than
in areas V2 and V3, and smaller than in area V6A (see Fig. 1).
The RF size in area V6 increases with eccentricity (Fig. 2), as in
all other prestriate areas, but they remain on average smaller than
in V6A and larger than in V2 and V3 at any value of eccentricity
(Fig. 3). Note that the data reported in Fig. 3 were all collected by
the same laboratory, hence their comparison should be quite
reliable. The differences in RF size indicated by the regression
lines of Fig. 3 turned out to be statistically highly signi®cant
for all comparisons (ANCOVA, P < 0.0001) and were used as a
further criterion to assign recorded cells to the different prestriate
areas.
Besides being correlated to the eccentricity, the size of RFs in V6
turned out to also be correlated to the ®eld representation, as shown in
Fig. 2B. We divided V6 RFs into two populations according to the
location of their centre in the upper or lower visual ®eld. The
regression lines of the two populations showed about the same slope
but signi®cantly different values of intercept. This means that RFs
located in the upper visual ®eld were on average larger than those in
the lower visual ®eld, at any value of eccentricity (ANCOVA,
P < 0.0001).
Figure 4 shows the retinotopic distribution of the RF centres and
the outline of the most peripheral RF borders of the same group of V6
cells reported in Fig. 2. It is evident that the whole contralateral
hemi®eld is represented in V6. Both the central part of the visual ®eld
and the periphery, up to ~ 80 ° of eccentricity, are well represented.
There is a prevailing representation of the lower visual ®eld with
respect to the upper one. The reasons for the under-representation of
the upper visual ®eld, particularly for its central part, will be
discussed later on in this paper.
Brain location of area V6
Figure 5 shows the cortical regions where V6 cells were recorded
from a typical case (16R). V6 cells were found in the medial surface
of the hemisphere (Fig. 5A), in the anterior bank and fundus of POS
(Fig. 5B±D), in the lateral part of the posterior bank of POS (Fig. 5D
and E), and in the dorsal wall of the medial parieto-occipital sulcus
(POM; Fig. 5B±D). Thus, area V6 occupies a `C'-shaped belt of
cortex orientated in the brain in a coronal plane. The upper branch of
this `C'-shaped belt of cortex is located in the POS and the lower one
in the POM, with the medial surface of the brain as a zone of junction
between the two. Laterally, the upper branch of V6 moves down from
the anterior bank to the fundus of POS (Fig. 5C and D), and then up
along the posterior bank of POS (Fig. 5D and E) where it merges into
the cortex of area V3.
Dorsally and anteriorly, area V6 borders continuously on area
V6A, from the medial surface of the hemisphere (Fig. 5A), through
the anterior bank (Fig. 5B and C), and fundus (Fig. 5D and E) of POS
(see also Galletti et al., 1999). Ventrally and posteriorly, area V6
borders on area V3: along the border between cuneate and precuneate
gyri, medially (Fig. 5B), along the caudal end of POM in the ventral
convexity of the brain (Fig. 5C), and along the fundus and posterior
bank of POS laterally (Fig. 5C±E).
In all our cases, the fundus of POS splits into two branches a few
millimetres laterally to the interhemispheric midline (see arrowheads
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
3926 C. Galletti et al.
FIG. 6. Brain location, extent and limits of area V6 in case 15L. Details and abbreviations as in Fig. 5.
in Fig. 5D and E). The anterior branch of POS (see arrowhead on the
left in Fig. 5D and E) is the result of a sharp bending, anteriorly, of
the POS fundus (Fig. 5C and D), that then continues into the fundus of
the lunate sulcus (LS) more laterally (Fig. 5E). The posterior branch
of POS (see arrowhead on the right in Fig. 5D and E) is the original
POS fundus that continues medio-laterally at about the same anteroposterior level (Fig. 5C and D), and then dies 6±8 mm away from the
interhemispheric midline (Fig. 5E). As shown in Fig. 5D and E, area
V3 occupies most of the cortex around the posterior branch of the
POS, while area V6 occupies the large fundus of POS, between its
two branches, as well as the posterior wall of the anterior branch of
POS, just in front of area V3. The lateral edge of area V6 in the POS
is often recognizable even macroscopically. It is located more or less
at the level where the posterior branch of POS collapses and the
anterior branch continues in the LS, in a cortical region that
represents the most medial appendix of the annectant gyrus (Fig. 5E).
This region appears as a tongue of cortex arising from the fundus of
the POS and merging into the cortex of the posterior wall of the POS
(Fig. 5D and E).
Case 16R is representative of two out of the ®ve hemispheres we
studied (14L and 16R). In two other cases (13L and 15L), the cortex of
cuneate and precuneate gyri remained separated from each other as far
as 5±6 mm away from the interhemispheric midline (Fig. 6A±C).
Accordingly, the upper and lower branches of the `C'-shaped V6
cortex remained in continuity through the cortex of the ventro-caudal
tip of the precuneate gyrus as far as 5±6 mm laterally to the
interhemispheric midline. Also, due to the separation between cuneate
and precuneate cortices, area V6 contacted V3 only at the lateral end of
POS, where the occipital cortex ®nally merged into the parietal one
(Fig. 6D and E). When cuneate and precuneate cortices merged
together, the posterior branch of POS became recognizable (see left
arrowheads in Fig. 6D and E), and it also became evident that V3
occupied the posterior branch of POS as in the other cases. Laterally,
area V6 occupied the fundus and the posterior bank of the anterior
branch of POS (see right arrowheads in Fig. 6B±E), as in the other
cases. Again as in all other cases, area V6 was bordered anteriorly by
V6A and posteriorly by V3.
The ®fth hemisphere we studied (case 16L) showed a signi®cantly
different gyral morphology. In this case (Fig. 7), the caudo-ventral tip
of the precuneate gyrus was absent while an additional amount of
cortex was present in the corresponding region of the cuneate gyrus,
in the occipital pole (Fig. 7A). According to these morphological
differences, area V6 occupied the additional amount of cortex in the
cuneate gyrus (Fig. 7A and B). Apart from this peculiarity, and in
spite of the different gyral morphology, area V6 occupied a `C'shaped belt of cortex as in the case shown in Fig. 5, with the dorsal
branch in the POS and the ventral one in the POM (Fig. 7B±D).
Again, similarly to the case shown in Fig. 5, area V6 bordered
anteriorly with area V6A and posteriorly with area V3. In the case
shown in Fig. 7 the anterior and posterior branches of POS were
dif®cult to recognize (see their probable positions indicated by
arrowheads in Fig. 7C and D). Anyhow, as in the cases of Figs 5 and
6, the anterior branch was occupied by V6 and the posterior one
by V3.
Visual topography of area V6
In order to study the visuotopic organization of area V6, we analysed
the RF sequences of V6 cells recorded along the same penetration, as
well as along nearby penetrations reconstructed on the same or
nearby brain sections. Figures 8±16 are examples of this study.
Figure 8 describes in detail the visual topography of V6 in case
16R. As illustrated by penetrations reported on section A, the region
of V6 located on the medial surface of the hemisphere showed a wellde®ned retinotopic organization. In this region of V6, RFs occupied
the peripheral part of the visual ®eld. They moved from the lower to
the upper visual ®eld along each penetration, constantly crossing the
horizontal meridian along the way (see RFs number 6 in penetration
`a' and number 10 in `b'). The eccentricity of RFs progressively
decreased along the penetration, so that they were more eccentric in
the lower than upper ®eld representation.
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
Visuotopic organization of area V6 3927
FIG. 7. Brain location, extent and limits of area V6 in case 16L. Details and abbreviations as in Fig. 5.
As reported above and illustrated in Fig. 5, the part of area V6
located on the medial surface of the brain continues into the anterior
bank of POS dorsally and the upper bank of POM ventrally. The RF
sequences of penetrations `a', `b' and `c' in Fig. 8 show that the lower
visual ®eld is represented in the upper branch of this `C'-shaped belt
of cortex, while the upper visual ®eld is represented in the lower
branch of V6. Accordingly, the horizontal meridian representation is
located in-between, running rostro-caudally on the medial surface of
the brain, more or less parallel to the lip of POM (sites 6 and 10 in
penetrations `a' and `b', respectively, and 8 in `d').
Figure 8 also shows that moving medio-laterally in the upper
branch of V6, RFs move from the periphery towards more central
representations. The central-most RFs (less than 20±30 ° in
eccentricity) were found in the posterior bank of POS, where the
V6 cortex merges into the cortex of V3 (penetration `e', and sites 1
and 2 in penetration `f'). Penetrations through this cortical region
showed RFs that moved from the horizontal meridian posteriorly, at
the border with area V3, to the vertical meridian anteriorly. Note that
laterally to section C of Fig. 8, the cortex of the posterior wall of POS
merges into that of the fundus of this sulcus (see Fig. 5E). Thus, the
vertical and horizontal meridian representations of the posterior wall
of POS continue with the same representations in the fundus of this
sulcus (sites 3±6 in penetration `f' and sites 1±8 in penetration `g').
The lower vertical meridian represents the anterior limit of area
V6. It runs medio-laterally along the anterior bank of POS, at the
border between areas V6 and V6A (sites 1±4 in penetration `c' in
Fig. 8). Laterally, it bends downwards and reaches the fundus of POS,
again at the border with V6A (sites 3±6 in penetration `f'). Then,
following the above-described course of the upper branch of V6, it
rises along the posterior bank of POS in its lateral end (site 6 in
penetration `e') reaching the central-most representation of V6.
The horizontal meridian representation is at the ventral, posterior
limit of area V6, at the border with area V3. The V6±V3 border
represents the central 40 ° degrees of the horizontal meridian (more
peripheral representations being on the medial surface of the
hemisphere, as described above) and runs medio-laterally along the
fundus of POS (site 1 in penetration `d', sites 1±8 in penetration `g').
Then, it rises along the posterior bank of this sulcus to reach the
central-most representation of V6 at the lateral end of POS (site 1 in
penetration `e').
Figure 9 summarizes the visual topography of area V6 in case 16R.
The ®gure shows aggregate ®eld outlines obtained by grouping cells
from separate microelectrode penetrations carried out in different
parts of area V6. It con®rms the retinotopic organization of V6, and in
particular: (i) the lower visual ®eld representation is located in POS
and the upper one in POM; (ii) the central representation is located in
the most lateral part of the posterior bank of POS; (iii) the vertical
meridian representation is located at the border with area V6A and
the horizontal one at the border with area V3.
The fact that on the medial surface of the hemisphere area V6 abuts
V3 was an unexpected ®nding, as in the literature it has been
repeatedly reported that the dorsal aspect of V3 does not reach the
medial surface of the hemisphere, but terminates into the parietooccipital cleft (Van Essen et al., 1986; Gattass et al., 1988). In our
cases, the V3 belt surrounded anteriorly area V2 in the LS and POS,
in agreement with the literature, as well as in the ventral convexity of
the brain, a ®nding previously not reported. Figure 10 illustrates this
aspect in case 16R. Medially (section 6), V2 occupied almost the
entire posterior bank of POS, and V3 the ventral-most part of the
cuneate cortex. The V2±V3 border was in the fundus of POS and
represented the horizontal meridian (sites 6±7). This cortical region,
at the junction between cuneate and precuneate cortices, also
represented the border between areas V3 and V6 (sites 7±8 versus
14±15). Area V2 extended from the POS to the medial surface of the
hemisphere and reached the stem of calcarine ®ssure (CAL), where it
was sandwiched between V3 ventrally and V1 dorsally (sites 11±13).
The V2±V1 border, within the CAL, represented the vertical meridian
(sites 12±13). The V2±V3 border, around the rim of CAL, probably
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
3928 C. Galletti et al.
a
contralateral visual field
b
12
17
10
6
80°
5
1
1
70°
c
d
7
5
1
1
8
4
g
e
6
1
8
1
f
3
1
2
6
FIG. 8. RF sequences in penetrations through area V6. (A±C) Parasagittal sections of the brain taken at the levels shown on the brain silhouette reported on the
bottom left of the ®gure. Letters `a' to `g' on the sections indicate the reconstructions of microelectrode penetrations passing through the occipital pole and
reaching the cortex of POS and POM in the depth. On the right, the reconstructions of the V6 RF sequences encountered along these penetrations are reported.
Thick lines join RF centres. The numbers along these lines, and along the reconstructed penetrations on the left, indicate the RFs and brain locations, respectively,
of some V6 cells. The RFs of `numbered' neurons are shown in grey. Other details and abbreviations as in Fig. 1.
represented the horizontal meridian, although we have no recordings
from this cortical region. We hypothesize that the horizontal meridian
representation (V2±V3 border) runs from the fundus of POS
anteriorly to the stem of CAL posteriorly, passing on the medial
surface of the hemisphere along the margin of the ventral convexity.
About 1 mm laterally to section 6 in Fig. 10 (section 9), the V2±V3
border rose up along the posterior bank of POS, still representing the
horizontal meridian (sites 4±5). At this parasagittal level, area V3 was
partly within the POS (sites 5±8) and partly in the ventral convexity
of the brain, at the posterior end of POM (sites 9±12). The orderly and
complementary visuotopic organization of these two parts of V3
support the idea that around the medial surface of the hemisphere V3
moves from the POS, dorsally, to the POM, ventrally, remaining
sandwiched between V2 and V6 in both the POS and the ventral
convexity of the brain.
Figure 11 shows the visuotopic organization of the part of V3
located in POS in the ventral convexity of the brain, in case 16R.
In the POS, V3 represented the central 30 ° of the contralateral
lower visual quadrant. In the ventral convexity of the brain, V3
represented most of the remaining periphery. The central
representation of V3, in the POS, was lacking in the representation of the central 5±10 ° of the visual ®eld that is well known to
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
Visuotopic organization of area V6 3929
FIG. 9. Visual topography of area V6 in case
16R. (Left) Parasagittal sections of the brain
taken at the levels shown on the brain
silhouette reported on the bottom right of the
®gure. The numbers on the sections within the
limits of area V6 indicate the cortical regions
whose cells had RFs in the corresponding
numbered parts of the visual ®eld shown in the
right part of the ®gure. Sections 6, 12, 16 are
the same as (B±D) in Fig. 5 and (A±C) in
Fig. 8. (Right) Outlines of the most peripheral
RF borders of groups of V6 cells recorded
from the cortical regions indicated by the same
numbers in the brain sections, in the left part
of the ®gure. Other details and abbreviations
as in Fig. 1.
be present in the part of V3 located in the posterior bank of LS
(Van Essen & Zeki, 1978; Burkhalter et al., 1986; Gattass et al.,
1988). Present data, together with those from literature, suggest
that the dorsal aspect of V3 is a topographically organized belt of
cortex that represents ~ 50 ° of the contralateral lower visual ®eld.
Area V3 is located in the depth of LS and POS as well as in the
ventral convexity of the brain, and surrounds V2 along all its
extent.
The same type of analysis described in Figs 8±11 for case 16R was
carried out in all the other cases we studied. Although some
differences were observed among the cases, the basic visuotopic
organization of area V6 remained that described above.
Figure 12 shows some penetrations in two different cases (13L and
14L). Penetrations `a' and `b', carried out in the medial region of
brain 13L, show that: (i) the vertical meridian was represented at the
border between areas V6 and V6A; (ii) the RF progression in V6 was
from the vertical to horizontal meridian; and (iii) the RFs in V6A
jumped from one part to another of the visual ®eld. Penetrations `c'
and `d', carried out in the lateral part of the POS in brain 14L, show
that: (i) area V6 merged into V3 in the ventral part of the posterior
bank of POS; (ii) the anterior border of V6 represented the vertical
meridian and abutted area V6A; and (iii) RFs in V6A jumped from
one part to another of the visual ®eld. All these results are in
agreement with those showed in case 16R.
Figure 13 illustrates the visual topography of V6, and of
neighbouring areas V2 and V3, in the most lateral part of POS in
case 14L. When moving dorso-ventrally along V2, in the posterior
bank of POS, RFs moved from the vertical to a more peripheral
horizontal meridian representation (®elds 1±3). At the V2±V3 border,
RF size suddenly increased and the progression of RFs reversed,
moving this time from the horizontal to vertical meridian (®elds 4±7).
V3 occupied the cortex around the posterior branch of POS, in the
deepest part of the sulcus. V6 occupied the posterior wall of the
anterior branch of POS. The locations of both areas are in agreement
with those shown in case 16R. Moving caudo-rostrally within area
V6, the RFs moved from horizontal to vertical meridian (®elds 8
versus 10; 9 versus 11 and 12). Moving dorso-ventrally, RFs moved
from central to peripheral parts of the visual ®eld (®elds from 8 to
13). The RFs of V6 neurons located along the border with area V3
re¯ected the topography of V3 itself. As a matter of fact, in both areas
they were located near the horizontal meridian dorsally (®elds 8 and 9
in V6 versus 4 in V3) and near the vertical meridian ventrally (®eld
13 in V6 versus 7 in V3). On the whole, in the posterior bank of POS
area V6 covered the central 20±30 ° of the lower contralateral visual
quadrant, about the same region of visual ®eld represented in the
lateral part of POS in case 16R.
Figure 14 shows some penetrations carried out in case 15L. Also in
this case the vertical meridian was represented along the border
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
3930 C. Galletti et al.
FIG. 10. Visual topography of areas V2 and V3 in the medial region of the brain in case 16R. Two parasagittal sections are shown on the left, taken at the levels
indicated on the brain silhouette reported at the top of the ®gure. Triangles, open and full circles and crosses on the sections indicate recording sites in V1, V2, V3
and V6, respectively; the RFs mapped at these recording sites are shown with the same numbers on the right. V6 RFs are indicated with dashed lines. Large, open
circles on the sections indicate locations of electrolytic lesions carried out at particular recording sites. Dashed lines on the sections mark the limits between
different cortical visual areas.
Ipsi
Contra
60°
V3
POS
V3
ventral
convexity
50°
FIG. 11. Visual ®eld representation of V3 in POS and the ventral convexity of
the brain. The shaded areas were obtained by delineating the external borders
of superimposed RFs of V3 neurons recorded in POS and in the ventral
convexity of the brain, respectively, in case 16R.
between areas V6 and V6A (penetrations `b', `c', `d'). Medially
(section 59; penetration `b'), while the electrode advanced into the
grey matter V6 RFs moved away from the vertical meridian. Moving
medio-laterally along the fundus of POS, the RFs of V6 moved from
the periphery towards more central parts of the visual ®eld
(penetrations `b', `c', `d'). The more central RFs were again found
where a tongue of cortex arised from the fundus of POS and reached
the posterior bank of the sulcus, to merge into the cortex of V3 in the
most lateral part of POS (penetration `d'). Areas V3 and V6 at this
level showed a similar visuotopic organization (penetration `d'). All
these data are in agreement with those of the other cases.
Figure 15 shows some penetrations in a case (16L) with a
completely different gyral morphology with respect to those
described in Figs 8±14. Many similarities and some differences have
been observed. In the lateral part of POS (section 19), area V6 was in
the fundus of the sulcus, as usual, but in this case V6 continued a few
millimetres along the fundus of LS, together with area V6A that
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
Visuotopic organization of area V6 3931
FIG. 12. Microelectrode penetrations through the cortex of POS in cases 13L and 14L. All details as in Fig. 1.
FIG. 13. Visual topography of areas V2, V3 and V6 in the lateral part of POS.
All details as in Fig. 10.
rostrally abutted V6 (sections 23, 27). The V6±V6A border
represented the vertical meridian (penetrations `a' and `e'), as usual.
Again as usual, the lower visual ®eld of V6 was represented in the
POS and the upper one in the POM (penetration `b'). Posteriorly, V6
bordered with V3, in POS as well as in POM. In the posterior end of
POM, the V3±V6 border represented the horizontal meridian
(penetration `d'), as in the most medial part of the brains of the
other cases. In the posterior branch of POS and in the fundus of this
sulcus, the V3±V6 border represented the vertical meridian (penetrations `b', `c' and `f'), contrary to that observed in the other cases.
However, more laterally, at the end of POS and the medial-most part
of LS, in the region where V3 and V6 cortices merged together, the
visuotopic organization of these two areas was similar: both V3 and
V6 showed RFs near the horizontal meridian dorsally and the vertical
meridian ventrally (penetrations `e' and `f'). This is the same
visuotopic organization observed in the other cases in the lateral-most
part of POS. Penetration `e' also shows that RFs increased in
eccentricity moving dorso-ventrally along the central representation
of V6, as in the other cases. The fact that in case 16L area V3 merges
into V6 in the medial part of LS, instead of in the lateral part of POS,
is probably due to the lateral extension of the posterior branch of POS
into the LS in this case. Anyhow, even in case 16L area V6 merges
into V3 more or less where the posterior branch of POS dies, and
even in this case this part of V6 contains the representation of the
central 30 ° of the contralateral lower visual quadrant.
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
3932 C. Galletti et al.
FIG. 14. Microelectrode penetrations through the cortex of POS in case 15L. All details as in Fig. 1.
Figure 16 shows the overall visual topography of V6 in the
`anomalous' case 16L. The lower visual ®eld is located in POS and
the upper one in POM as in all other cases. The lower vertical
meridian is at the border with area V6A as usual. The horizontal
meridian is at the border with area V3 in the medial part of the brain.
Laterally, the topography is more complex (see comments on
Fig. 15). The most lateral part of area V6 enters into the medial
end of the LS (section 27). Here, V6 topography matches that of V3,
with the horizontal meridian representation dorsally (1A) and the
vertical one ventrally (1B). Note that laterally to section 27, the V6
cortex labelled 1A (representing the horizontal meridian) merges into
the V3 cortex located just above it, representing the horizontal
meridian too (see penetration `e' in Fig. 15). The central-most
representation of V6 is located in the most lateral part of this area, as
in all other cases.
On the basis of the data collected during microelectrode
penetrations, we have tried to reconstruct the brain location and
visuotopic organization of area V6 on three-dimensional models of
the brain. Figure 17 shows the result of this work on the most typical
and studied case 16R. Figure 17A shows the parieto-occipital cleft
open. The upper branch of V6 occupies the ventral part of the anterior
bank of POS, the fundus and the most lateral part of the posterior
bank of POS. Note that in the ®gure the most lateral part of V6 covers
a part of area V3, that remains beneath the V6 cortex. Figure 17B
shows the cortex between the two branches of V6 (on the medial
surface of the hemisphere), as well as part of the lower branch of this
area (in the dorsal wall of POM).
Note that the locations of the lower and upper visual ®eld
representations, the vertical and horizontal meridians, and the centralmost representation of the visual ®eld reported in Fig. 17 are
according to the above-described retinotopic organization of area
V6 (see Figs 8±16). The small emphasis of central ®eld representation
with respect to the periphery is evident, although the whole visual
®eld turns out to be represented. Note also that the isoeccentricity
lines of the lower visual ®eld run obliquely along the anterior bank of
POS. This explains why penetrations in parasagittal planes through
this cortical region show RF sequences that progressively decrease in
eccentricity (see Fig. 8, sites 1±5 in penetration `a' and 1±10 in
penetration `b'). On the other hand, the oblique running of
isoeccentricity lines allows the V6 RFs to remain topographically
in register with the RFs of V6A dorsally and those of V3 ventrally,
along the common borders of these two areas with area V6. In fact,
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
Visuotopic organization of area V6 3933
FIG. 15. Microelectrode penetrations through the cortex of POS, POM and LS in case 16L. All details as in Fig. 1. Sections 19, 23, 27 are the same as C±E in Fig. 7.
the visual cells of the ventral-most parts of area V6A have RFs in the
far periphery (Galletti et al., 1999), while those in the region of V3
abutting area V6 in the POS are much more central (see Fig. 11).
Discussion
Area V6 is a cortical visual area interposed between areas V3 and
V6A in the macaque brain. Previous studies reported the existence of
V6 in the anterior bank of POS (Galletti et al., 1996). Present results
indicate that this area is located in the depth of POS and POM, as well
as in the caudo-ventral tip of the precuneate gyrus, on the medial
surface of the hemisphere. The cortical extent of V6 on the medial
surface of the hemisphere is strictly dependent on gyral morphology,
changing largely from one case to another. Completely new is the
®nding that part of V6 is located in the posterior bank of POS.
Area V6 is retinotopically organized. It contains a topographic
representation of almost the entire contralateral visual ®eld, with the
lower visual ®eld in the POS and the upper one in the POM, the
periphery represented medially in the brain and the centre laterally.
Although both central and peripheral parts of the retina are
represented in V6, the central representation is not magni®ed, as is
on the contrary usual in all other cortical visual areas.
Comparison of areas V6 and PO
As suggested in a previous paper (Galletti et al., 1996), area V6 might
correspond to the area PO that Colby and co-workers described in
anaesthetized and paralysed macaque monkeys (Colby et al., 1988).
Like area PO, V6 occupies the ventral aspect of precuneate gyrus,
represents the lower visual ®eld in the anterior bank of POS and does
not have an expanded representation of central vision. However,
present results show that a number of differences are evident between
the two areas. For instance, the upper ®eld representation of area V6
involves most of the dorsal wall of POM, going into the depth of the
sulcus up to several millimetres away from the interhemispheric
midline. In contrast, the upper visual ®eld in PO has been reported to
be entirely represented on the medial surface of the hemisphere (see
®g. 1 of Colby et al., 1988). Accordingly, the representation of the
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
3934 C. Galletti et al.
FIG. 16. Visual topography of area V6 in case
16L. Details and abbreviations as in Fig. 9.
Sections 14, 19, 27 are the same as B, C and
E in Fig. 7.
horizontal meridian in PO runs dorso-ventrally along the anterior
bank of POS, while in V6 it runs medio-laterally along the fundus of
POS.
Another example of differences between PO and V6 is the location
of central ®eld representation. In PO, the central-most RFs (below
30 ° of eccentricity) were found in two separate sites in ventral and
lateral parts of the anterior bank of POS, respectively (Gattass et al.,
1985). In V6, the central representation is unique and RF centres
below 20 ° of eccentricity were exclusively found at the lateral end of
the posterior bank of POS. Because the central-most RFs in V6 were
more central than those found in PO, it could be that the disagreement
is at least partially due to differences in the extent of recording
regions. In other words, the regions of central representation in PO
could actually be part of area V6, but the central-most representation
of V6 was probably outside the recording site of Gattass et al. (1985).
In support of this view is the fact that we too found RF centres with
eccentricity of 30 ° or less in the lateral part of the fundus of POS (see
Fig. 8, penetrations `f' and `g'; Fig. 12 penetration `d'; Fig. 14
penetration `c'; Fig. 15 penetration `c'; Fig. 17), that is in the region
where Gattass and co-workers found their central representations.
A third difference between PO and V6 regards the overall
topographical organization of the two areas. PO is reported to have a
complex visual topography in that it does not conform to the retinal
surface (Gattass et al., 1985). In contrast, the visual topography of V6
is quite orderly, as summarized in Fig. 17. The RFs of cells recorded
along single penetrations through V6 moved on average in a coherent
direction, according to the orderly visuotopic organization of this area.
This behaviour was in strong contrast not only with that reported for
area PO, but also with that observed in area V6A, a cortical region that
completely surrounds area V6 dorsally and anteriorly (see ®g. 9 of
Galletti et al., 1999). The RF locations of V6A visual neurons showed
very large scattering in parasagittal penetrations through this area,
jumping repeatedly in completely different parts of the visual ®eld (see
penetrations `c' in Fig. 1; `a' and `c' in Fig. 12; `a' in Fig. 14; see also
Galletti et al., 1999). This behaviour of V6A cells might help in
explaining the differences observed between the visual topography of
areas V6 and PO. As fully discussed in a previous paper (Galletti et al.,
1996), the antero-dorsal border of area PO, as de®ned by myeloarchitecture, might include the caudo-ventral part of area V6A. If this was
the case, the complex topography of area PO could be the result of
V6A contamination, that would add a non-topographic representation
of the retina to the topographic one of area V6.
The representation of the central upper ®eld in area V6
Area V6 contains an almost complete representation of the
contralateral visual ®eld. However, while the central representation
of the lower visual ®eld was unequivocally found at the lateral end of
the posterior wall of POS, that of the central upper visual ®eld was
substantially missed (see Fig. 4). The reason for this is not clear.
Given that it is unlikely that this sector of the visual ®eld is not
represented in V6, a possible explanation is that we have missed
recording from there. Actually, it was not easy to reach the cortical
region where the upper visual ®eld was represented. V6 cells with
RFs located in the upper visual ®eld were found in a relatively small
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
Visuotopic organization of area V6 3935
FIG. 17. Retinotopic organization of area V6.
(Left) Dorsal view of the brain in the region of
POS. In the enlargement shown in A, the POS,
LS and IPS are shown opened to reveal the
cortex buried within them (dark grey area).
Area V6 in the parieto-occipital cleft is shown
in a lighter grey. Filled and empty circles
indicate the representation of the horizontal
(HM) and vertical (VM) meridians of area V6,
respectively; the star, the centre of gaze (F).
The dashed lines are isoeccentricity lines. The
`minus' sign indicates the lower visual ®eld
representation. The dotted lines are the borders
between different cortical areas, according to
the present as well as previous results (see
Galletti et al., 1999). V2, V3, V6, V6A, areas
V2, V3, V6 and V6A. (Right) Medial view of
the hemisphere in the region of POM. In the
enlargement shown in B, the cortex of the
cuneate gyrus is pulled back and down to
show part of the dorsal wall of POM. The
`plus' sign indicates the upper visual ®eld
representation. Other details as in A.
strip of cortex in the upper wall of POM, located more than 10 mm
away from the entry point of the electrode into the brain. Not all of
our penetrations reached the POM, thus data on this cortical region
were less numerous with respect to those from other regions of V6.
For these reasons, we cannot exclude having missed recording from
the cortical region representing the central part of the upper visual
®eld.
An alternative explanation is that the central upper-®eld representation of V6 is not located in the POM, but in another region of the
brain not explored in our experiments. To this regard, some data from
the literature suggest an intriguing hypothesis. Van Essen & Zeki
(1978) originally described area V3A as a strip of cortex located in
the LS, containing both lower and upper ®eld representations of the
central 20±25 ° of the visual ®eld. They also reported the ®nding of an
anomalous `second' central ®eld representation of V3A medially, in
the lateral end of POS, in a location where they would have expected
to ®nd the representation of the far periphery of V3A. This secondary
representation of V3A (medial V3A) encompasses the central 20±25 °
of the retina, both in the lower and upper contralateral quadrants. The
authors questioned whether this secondary central representation
could form part of an unidenti®ed additional visual area. As a support
to this hypothesis, the same authors found that the V3A in the LS had
RFs `reasonably small', while the medial V3A had RFs `large even
when they overlap the fovea' (Van Essen & Zeki, 1978, p. 214). It
seems reasonable to suppose that the medial V3A is actually the
central representation of area V6. As far as the lower quadrant
representation is concerned, the brain location of the medial V3A and
that of the central V6 is the same, in the posterior wall of the lateral
end of POS; in addition, the sector of the visual ®eld they represent is
more or less the same (central 20±25 °) and the RF size is of the same
order of magnitude. As far as the upper quadrant representation is
concerned, it is located anteriorly to the lower one, between the
lateral end of the POS and the caudal end of the IPS (see ®gs 9 and 10
from Van Essen & Zeki, 1978), in a cortical region not explored in
our experiments; the sector of the upper visual ®eld the medial V3A
represents (central 20±25 °) is complementary to that represented in
the upper-®eld representation of V6 located in the POM; ®nally, the
RF size is of the same order of magnitude as the central ®eld
representation in V6. For all these reasons, we believe it likely that
the medial V3A is actually the central ®eld representation of V6. We
also suggest that the posterior intraparietal area (PIP), that has been
described as occupying the same cortical region of the medial V3A
and is reported to contain both upper- and lower-®eld representations
(Colby et al., 1988), is actually the central representation of area V6.
Functional considerations
The present results show that area V6 contains an orderly, retinotopic
map of the visual ®eld, with an emphasis for the periphery
representation and a more detailed representation of the lower visual
®eld with respect to the upper one. V6 cells respond briskly to visual
stimulations, are very sensitive to orientation, direction and speed of
movement of visual stimuli, and many of them are sensitive to
oculomotor activity (Galletti et al., 1991, 1995, 1996). The visuotopic
organization and cells' characteristics of V6 suggest a number of
possible functional roles for this area. For instance, it could be
engaged in the analysis of the ¯ow ®eld resulting from self-motion,
and/or play a role in selecting peripheral targets in visual searching. It
could also be engaged in the control of arm-reaching movements
towards non-foveated targets. The strong anatomical connection of
V6 with area V6A (Matelli et al., 1995; Shipp & Zeki, 1995; Shipp
et al., 1998) seems to support this view. V6A contains cells able to
directly encode visual space (Galletti et al., 1993, 1996) as well as
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 3922±3936
3936 C. Galletti et al.
arm-reaching neurons (Galletti et al., 1997), and is strongly connected
with the dorsal frontal cortex involved in planning arm movements
(Matelli et al., 1998; Shipp et al., 1998). The V6±V6A±dorsal area 6
pathway could be engaged in eye±hand coordination during arm
reaching towards objects in the peripersonal space. We suggest that
area V6 provides V6A with the visual and oculomotor information
needed for this visuomotor processing.
Acknowledgements
The authors wish to thank L. Sabattini and G. Mancinelli for mechanical and
electronic assistance, and S. Boninsegna for technical assistance during
experiments. This work was supported by Grants from Ministero dell'UniversitaÁ e della Ricerca Scienti®ca e Tecnologica and Consiglio Nazionale delle
Ricerche, Italy.
Abbreviations
CAL, calcarine ®ssure; IPS, intraparietal sulcus; LS, lunate sulcus; PIP,
posterior intraparietal area; PO, parieto-occipital area; POM, medial parietooccipital sulcus; POS, parieto-occipital sulcus; RF, receptive ®eld; SPL,
superior parietal lobule.
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