Opinion

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TRENDS in Neurosciences Vol.26 No.1 January 2003

Improbable areas in the visual brain

S. Zeki
University College London, London WC1E 6BT, UK

Recent results from anatomical, physiological and

imaging experiments cast doubt on the existence of
some areas in the primate visual brain and call for a
much overdue re-assessment of what is a conceptually
highly unsatisfactory view of how the primate visual
brain is organized, a view that has survived more or
less unscathed for at least 15 years and has been
embraced uncritically by a significant element in the
human brain imaging community. That view can be
summarized as follows: that there are areas in the
visual brain that represent only one quadrant of the
visual field, leaving the other quadrant of the hemifield
unrepresented, or represented in another area, leading
to what Jon Kaas has called improbable areas. It is
not the improbability of such a view that is surprising;
rather, it is its ready acceptance on the basis of
questionable evidence.
The right half of the visual field is represented in the left
brain hemisphere, and vice versa, the two separate
representations being unified by a commissure that links
the two cerebral hemispheres, the corpus callosum (Fig. 1).
The discovery of many visual areas in the brain [1 4] with
the promise of more to come, naturally raises the question
of which criteria should be used in conferring the status of
a visual area on a cortical zone. Two obvious ones are that
an area should be activated by visual stimuli and should
have an independent and more or less complete map of the
contralateral visual field, to include both the upper and
lower quadrants. This is so, even if a given quadrant, or
part of the retina, claims a disproportionately large space
in a cortical area, as happens even at the level of the
primary visual cortex (V1). To this can be added other
features, such as a distinct set of anatomical (including
callosal) connections, identifiable and unique functional
properties [1] and a distinctive architecture, although the
search for the latter has not always been fruitful. In 1986,
Van Essens group [5] proposed a radical departure from
this list by purporting to show that one of the areas
constituting the visual brain, area V3, does not have a
complete representation of the visual field, as had been
supposed from earlier anatomical studies [6,7]. Instead,
they conceived of this area, which occupies a narrow strip
anterior to area V2 (Figs 1 and 2) as consisting of two
different areas a dorsal one called V3 and a ventral one
known as VP each representing one quadrant only of
the contralateral hemifield. They proposed this even
though the retinotopic map in VP in both the human
[8 10] and the monkey [3,11] is a mirror image of that in
Corresponding author: S. Zeki (zeki.pa@ucl.ac.uk).

upper V3 (Fig. 1). The separation into two distinct areas

was based on the supposition that lower V3, unlike its
upper counterpart, not only lacks a direct anatomical
input from V1, but also has a high proportion of colourselective cells [5]. The implication was obvious: VP is an
area registering activity only in the upper contralateral
quadrant, without the capacity to register the same
activity (including, above all, colour) when it occurs in
the lower contralateral quadrant or leaving it to some
other improbable area, one registering activity in lower
quadrant alone, to do so. This, in turn, leads to the
supposition that there could be other improbable areas in
which only one quadrant of the visual field is represented
(Fig. 3). This is odd: psychophysical experiments have
shown that some attributes are more readily perceived
when presented in one quadrant than in another [12,13],
but none has ever shown that an attribute can be perceived
only when presented in one quadrant alone.
In fact, the evidence against such improbable areas in
the visual brain is mounting. The notion that there is an
asymmetrical anatomical input from V1 to upper and
lower V3 was questioned years ago, when it was shown
that there is a direct input from V1 to lower V3 in Cebus

(a)

V1

Calcarine
sulcus

Corpus
callosum

(b)
V3
V2
V1
V2 V3
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Fig. 1. Representation of the visual field in visual cortex. (a) Representation of the
right hemifield in the primary visual cortex, V1. The upper quadrant of the hemifield (red) is represented below the calcarine sulcus, whilst the lower quadrant
(green) is represented above the calcarine sulcus. The corpus callosum is shown
in blue. (b) The representation of the visual field in visual areas V1 to V3, shades of
red and pink indicating representation of the upper quadrant and shades of green
indicating representation of the lower quadrant. The dotted lines show the representation of the horizontal meridian of the visual field (horizontal dotted line in
part a) in these visual areas. The solid lines between the areas show the representation of the vertical meridian.

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Opinion

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TRENDS in Neurosciences Vol.26 No.1 January 2003

V3A
V3
V1
V2

V4
Face and object
recognition areas

V5 (motion)
TRENDS in Neurosciences

Fig. 2. Areas of the visual brain. Areas V3 (dark blue), V3A (violet), V4 (red) and V5
(pink), and those of face and object recognition (blue), receive their input largely
from V1 (yellow) and V2 (green).

monkeys [14] and when detailed recording experiments

showed that there is a continuous representation of visual
fields in V3 from lower to upper quadrants as one proceeds
dorsoventrally [11]. Such findings, made in New World
monkeys, have been substantially reinforced by a more
recent study [15] showing that in the Old World macaque
monkey, too, there is a direct input from V1 to V3. That
study, with other supporting evidence [16], has led Lyon
and Kaas to conclude that V3 is one continuous area, not
two separate areas, and that it is characteristic of all
primates. Thus, one of the main criteria for separating V3
into two areas, namely an asymmetry in anatomical input
from V1, has lost its force.
The ready acceptance of such a subdivision in the
macaque, and its uncritical translation into the human
brain (in which the two corresponding areas have also been
called V3 and VP) is surprising, because all human
imaging experiments have shown that upper and lower
parts of V3 are activated in the same way [17]. This speaks
against its separation into two areas. More significantly,
no human imaging study has ever shown that human VP
is specifically or more vigorously activated with colour,
even when the question has been directly addressed [18].
The second criterion for separating V3 into two independent areas (namely, an emphasis on colour in VP) is, thus,

(a)

(b)

(i)

(ii)

TRENDS in Neurosciences

Fig. 3. Two theories of how a hemifield is represented in the brain. The coloured
quadrants on the screen (a) are represented in an arbitrary region in the contralateral side of the brain (b). (i) The conventional theory, which shows an orderly, continuous and more or less complete map of the contralateral hemifield. (ii) Van
Essens theory that such areas could be subdivided into two independent areas on
the basis of asymmetry in anatomical input and differences in function.
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V4

V4
'V4v'

TRENDS in Neurosciences

Fig. 4. A ventral view of the human brain showing the representation of the upper
visual field (red) and the lower visual field (green) in V4 and V4a, the latter a newly
discovered area within the human colour centre. Blue lines around V4 show the
position of V8 according to Hadjikani et al. [24]. Purple circles caudal to V4 show
the position of area V4v of Sereno et al. [7] and Hadjikani et al. [24], which has yet
to be shown to be a separate area [18]. Inset shows the visual field itself.

also weakened. The consensus of the evidence seems to be

that there is no justification for separating V3 into two
areas, on either anatomical or functional criteria. V3 is,
instead, one whole area, in which both upper and lower
fields are represented as was originally proposed.
The improbable becomes implicitly acceptable
A consequence of the unquestioning acceptance of the
separation of V3 into two areas has been the implicit
acceptance that there might be other such improbable
cortical areas in which only one quarter of the visual field
is represented. The advent of the phase-encoding method
[19] for mapping visual fields in human cerebral cortex
revealed, in some hands, an area V4v [20,21] located
posterior to the colour centre, area V4 (Fig. 4). The
attached v implies that the region maps the upper
contralateral quadrant only. No one seemed especially
concerned that the same method did not reveal V4d, the
dorsal counterpart that should represent the inferior
contralateral quadrant presumably because of the
implicit acceptance that improbable areas might, after
all, exist. In fact, V4v was thought to be distinct from the
ventrally located human V4, in which both contralateral
quadrants are topographically mapped [22], and damage
to which can lead to complete contralateral cerebral colour
blindness (hemiachromatopsia) [23]. The confirmation by
Hadjikhani et al. [24], that both contralateral quadrants

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25

previously defined visual area (Fig. 4). Heywood and

Cowey [25] accepted this claim of a new area uncritically.
They wrote that a newlydefined [sic ] color area had been
found and that it is this area, V8, rather than the favorite
candidate, V4, that, when lesioned, produces cortical
colour blindness. This led them unquestioningly to the
view that the human color center is distinct from area V4
(note how, in this uncritical acceptance, the small v has
been dropped from the equation). This is despite the fact
that the newlydefined color area has the same brain
coordinates as V4 (Fig. 4).
Does V4v exist?
In fact, V4 and the newlydefined color area not only share
the same coordinates, but also are both located anterior to
V4v. Tootell and Hadjikhani have since admitted [27] that
their new cortical area is, in fact, nothing more than the
previously defined colour centre but they have pleaded
that it should be called V8, because the fourth visual map
is constituted by their improbable area V4v. But does
such an area exist? We have not been able to find any
evidence for a separate area V4v. Nor, seemingly, have
others [28]. The question has been directly addressed by
Wade et al. in the most detailed topographic studies of the
human visual brain to date [17]. They could not find a
quarter-field representation corresponding to area V4v.
Instead, they found that V4 constitutes the fourth visual
map, abuts V3 and corresponds to the colour centre of the
human brain (Fig. 5). Thus, the argument for calling the
area V8 is etiolated. Given the evidence against brain
areas with only quarter-field representations, it is up to
the proponents of V4v to demonstrate its existence
convincingly or to withdraw it.

Fig. 5. A functional magnetic resonance imaging (fMRI) image of the ventral view
of the left hemisphere of the brain, showing the relative locations of V3 and V4. In
their recent, detailed mapping study of visual areas in the ventral cortex, Wade
et al. showed that area V3 directly abuts area V4, with no additional area (V4v)
between them (Wade et al., unpublished; figure kindly supplied by Wade et al. ).

are topographically mapped within human area V4 as

originally defined [25], reveals eloquently the confusion
[26] that is traceable in large measure to the blind
acceptance of the concept of visual areas with only a
quarter-field representation of the visual field. Hadjikhani
et al. showed, as we had before them [22], that there is a
complete representation of the contralateral hemifield
within the ventrally located colour centre, area V4. But
because of their belief in the existence of an area V4v that
is distinct from our V4 and which represents only the
upper contralateral hemifield, they imagined that they
had discovered a new retinotopic area that we call V8.
This previously undifferentiated cortical area was consistently located just beyond the most anterior retinotopic
area defined previously, area V4v (my emphasis on the v).
An examination of their results shows, however, that their
new retinotopic area has the same coordinates as our V4
and is, thus, nothing more than the re-discovery of a
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Precedence is finally used explicitly the case of KO

The acceptance of the improbable V4v was made possible
by the implicit acceptance of the improbable VP. But the
defunct and improbable VP has also been used explicitly
as a precedent for yet another improbable area, KO
(kinetic occipital area), claimed to be specialized for the
processing of kinetic contours [29]. Attempts are currently
being made to equate human KO with the dorsal part of
area V4 in the macaque, V4d. The improbability of such
an equation is reinforced by the improbability of the function imputed to KO from the evidence currently available.
V4d is the part of area V4 in the macaque that
represents lower visual fields but it has never been
considered to be a separate area. The equation of this
part of macaque V4 alone with human KO implies that
KO represents the lower contralateral visual fields only.
Recent evidence shows that KO is engaged in extracting
shapes from all sources and not from kinetic contours
alone [30]; it is, therefore, not specialized for kinetic
contours and, to avoid misleading functional names, is
thus better referred to as area V3B [31]. It would be
strange if such an area were to represent one quadrant
alone, for this would imply that it extracts contours in only
one quadrant an improbability. In fact, Smith et al. [31]
have concluded that V3B (KO) represents only the lower
contralateral visual field, but their figures could equally
well be interpreted to mean that V3B contains a complete

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TRENDS in Neurosciences Vol.26 No.1 January 2003

and independent representation of the entire contralateral

hemifield, with the lower quadrant claiming more cortical
space. Moreover, other retinotopic studies of human visual
cortex show that there is a complete representation of the
contralateral hemifield in V3B (KO) [18].
The equation of human V3B with only a part of monkey
V4 (dorsal V4 or V4d) would mean that human V3B and
monkey V4d are improbable areas even though the
evidence suggests that both human V3B and macaque V4
have a complete map of the contralateral hemifield V4d
being nothing more than the dorsal part of V4 in the
macaque. In trying to understand why such claims have
been so uncritically accepted, it becomes obvious that
precedent, and especially that of VP, has played a big role.
Tootell and Hadjikhani have written that Although such
separated quarter-field representations are conceptually
unsatisfying, they are not unprecedented: the quarterfield representations in macaque V3 and VP have long
been considered separate areas by some investigators,
based on empirical differences between V3 and VP [27].
But there are also many who do not accept such improbable areas, and the weight of evidence is on their side.
It is a wonder that so fragile a concept as that of visual
areas in which only a quarter of the visual field is
represented should have been so uncritically accepted
for so many years, and that so much should have been built
on such a flimsy view, even when much evidence speaks
against it. This view was largely erected on the basis of
area VP, but the evidence for such a separate area has
never been convincing. Of course, when the original
concept collapses, the rest follows, as with dominoes.
This is what we are witnessing today with the demise of
VP. Perhaps the traditional, and even conservative, view
of what constitutes a visual area has considerable merit
after all.

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