The visual association cortex

Semir Zeki

University College London, UK

The concept of visual association cortex derives from early myelogenetic

studies, assorted cases of so-called visual agnosia and much philosophical
speculation. A review of the evidence suggests that it is perhaps time to
review our concept of the visual association cortex.

Current Opinion in Neurobiology 1993, 3:155-159

Introduction scious awareness? Or was association intended to signify

The concept of association cortex is essentially a some-
what vague functional concept inferred from fairly pre-
cise anatomical studies. In time, philosophical specula-
tion came to make its contribution to the concept, es-
pecially in visual cortex. Not surprisingly, this served to
confuse the concept rather than illuminate it. However
that may be, the different approaches reinforced each
other and led to a fundamentally flawed view of the cere-
bral processes involved in vision. This supposed that the
function of visual association cortex was to ‘understand
what was seen, seeing being a function of the primary
visual cortex, area Vl. Any revision of the concept of vi
sual association cortex thus entails a profound revision
of our views not only of visual cortex and the processes
it undertakes, but also of our philosophical approach to
the problem of vision.
the unification of the representation of different points,
representing different regions of the body surface, in the
topographically organized sensory areas? Neurologists,
assuming them to have thought about the implications
of their terminology, remained vague about what they
meant by the term. Instead, they proposed a definition
that was so general that it applied to all the above cate-
gories. They imagined that it was association cortex that
gave visual ‘impressions’ their meaning and hence that
it was visual association cortex which dealt with ‘higher’
functions.

Definition of visual ‘association’ cortex

The human cerebral cortex is not fully differentiated at

birth. Some areas, which Flechsig [1,2] called ‘primor-
dial’ and amongst which he numbered the primary visual
cortex (area Vl), are myelinated at birth, though they
occupy only a small fraction of the total cortical surface
(Fig. 1). They are connected to the peripheral organs and
are separated from each other by other, and much larger, F&l. Flechsig’s diagram of the medial view of the human brain,
cortical areas. The latter are not connected to the periph- to show the primordial areas (hatched and cross-hatched) and
the association areas (in white). The visual association cortex was
eral organs and become myelinated at various stages after
considered to surround the primary visual cortex.
birth, as if their myelination depends upon the acquisi-
tion of experience. Flechsig used the term ‘association’
cortex to describe these latter areas, believing them to be Lissauer [ 31, whose speculations were to have a powerful
the Geistige Zentren or Cogitationszentren (mind centres influence on visual neurologists, anticipated the present
or psychic centres). Hence, the commonly used altema- talk about ‘lower’ and ‘higher’ levels of vision by us-
tive term for visual association cortex was the visuo-psy- ing Leibniz’s term ‘apperception’ to speak of the func-
chic cortex. Large cerebral areas, whose boundaries can tion of Vl in high sounding terms. Apperception was
be defined with fair precision, were thus inferred to have “....the highest degree of perception, in which the con-
a function, that of association, though the function itself sciousness accepts the sensory impression with maximal
was not precisely delined. Was it an association of present intensity” - a view which invests Vl with a critical role in
with past records in a given modality, such as vision, or consciousness. This was followed by the process of ‘as-
an association between different modalities that neurolo- sociation’, of “....connecting other conceptions with the
gists had in mind? Would it be the kind of association content of the perception”, thus giving them their mean-
that dignifies vision with meaning and therefore con- ing. But no one specified what these conceptions may

@Current Biology Ltd ISSN 0959-4388 155

156 Cognitive neuroscience
be or what underlying neural mechanisms to look for.
It was suficient that lesions within Vl led to blindness,
while those in the ‘visuo-psychic’ cortex led to the syn-
drome of mind blindness (seelenblindheit), later termed
agnosia, a condition in which a patient was deemed to
be able to ‘see’ but not to ‘understand’ what was seen.
This view, approved of by both Henschen and Holmes,
was well summarized by Campbell [4] in 1905 when
he spoke of two areas “ ...one specialized for the pri-
mary reception of visual sensations, and the other consti-
tuted for the final elaboration and interpretation of these
sensations”. Flechsig had believed, though without com-
pelling evidence, that the role of visual association cortex
was to associate visual signals with signals derived from
other sources, and endowed it with a certain level of
consciousness. Other neurologists, including Campbell;
Holmes and Henschen, had believed, again without much
evidence, that it would associate the received visual ‘im-
pressions’ with similar past ‘impressions’, thus leading to
‘understanding’. By the time neurophysiologists got hold
of the idea, they perpetuated the earlier views without
considering the evidence, which was in any case scant.
Thus, Clare and Bishop [5] studied an area well re-
moved from the primary visual cortex in the cat and
“inferred [it] to comprise an association area relating op-
tic and acoustic activity” although no acoustic activity was
studied there. In summary, these views - however much
they may have differed in detail - separated the process
of ‘seeing’ from that of ‘understanding’ and attributed a
separate cortical seat to each. It is this fundamental con-
cept that more recent work on visual ‘association’ cortex
has challenged.
The challenge to the concept of association
cortex
Perhaps the first step in the revision of this view came
from the demonstration that the visual association cor-
tex, far from being the single area which its uniform
architecture and relatively late myelination had implied,
consists in fact of multiple visual areas (for a review,
see [6] ). This demonstration raised the possibility that
the cerebral processes involved in vision are much more
complex than the one implied in the dual concept of the
early neurologists. The fundamental turning point came,
however, with the demonstration that the visual areas of
the ‘association’ cortex undertake different tasks, not the
same task at ever-increasing levels of complexity, as was
implicit in the earlier doctrine of exclusive hierarchies
[7,8]. Thus, area V5 is specialized for visual motion [9],
while area V4 is specialized for cblour and form in associ-
ation with colour [l&14]. V3, by contrast, is specialized
for dynamic form [ 15,161. A functional specialization is
also characteristic of the prestriate cortex of man [ 171,
but this is not to imply that the specializations enumer-
ated above are the only functions of these areas. That
the areas of the visual association cortex (now better re-
ferred to as the prestriate cortex) receive parallel inputs
from Vl [ 111, not only served to emphasize the fact that
the cortex undertakes several visual operations in par-
allel to construct the visual image in the brain, raising
the fundamental question of how the specialized visual
areas interact to provide the unitary visual image in the
brain, but strongly suggested that the functional segre-
gation evident in prestriate cortex would be mirrored
somehow in area Vl itself [ 111, even if the compelling
evidence for such a supposition was to come only sev-
eral years later [ 181. No one has been able to show that
the cells in the above prestriate areas are influenced to
any extent by stimuli belonging to another modality, say,
olfactory or auditory. Equally, no one has yet been able to
show that the memory of past visual experiences or stim-
ulation is crucial for the activation of cells in these areas,
which is not the same thing as saying that such influences
may not be found to be crucial in the future. Thus, the
speculations of the early neurologists, whether of Flech-
sig or of Holmes, concerning the ‘understanding’ cortex
do not gain much support from the current physiological
profile of the visual areas of prestriate cortex.
Does visual association cortex use a
fundamentally different strategy?
What is it that distinguishes the visual areas of the pre-
striate cortex from area Vl? Is it a qualitative difference
or a quantitative one? The single most striking feature of
prestriate visual areas is their specialization. While anyone
wanting to explore the functional organization of area Vl
or area V2 (which surrounds it) with an electrode will
encounter cells with many different properties [l’$-211,
even if cells dealing with a given attribute are grouped
together, the properties of cells in individual prestriate
areas are more homogeneous. The cells of area V5,
for example, are overwhelmingly directionally selective
and uninterested in colour, whereas those of area V4
are overwhelmingly wavelength selective [ 12-15,21,22].
The initial temptation therefore would be to suppose that
the role of prestriate cortex is to segregate or ‘dissociate’
signals rather than associate them. But the segregation of
visual signals belonging to different sub-modalities of vi-
sion is not a radically new strategy employed by the pres-
mate cortex, even if it was first demonstrated there. More
recent studies show that visual signals are also segregated
into sub-compartments in area Vl [IS], from which the
specialized areas receive their cortical input, as well as
in area V2, which surrounds area Vl and projects to
the same specialized visual areas [ 23-251. Hence, the
segregation of visual signals in the prestriate cortex is
not a novel strategy but a continuation of the strategy
employed at earlier levels of the visual pathways.
The next striking feature of the prestriate areas is that,
compared with the striate cortex, cells in the former
have larger receptive fields. This is almost certainly the
consequence of the need to collect information from
larger parts of the field of view. But this is not a strat-
egy developed in, or unique to, the visual areas of the
prestriate cortex. Indeed it is a hallmark of the visual
pathways in general. The simple cells of the striate cor-

tex have larger receptive fields than those of the lateral
geniculate nucleus from which they receive input, and the
complex cells have larger fields still [ 71. The strategy is
continued well beyond the prestriate cortex, for cells in
the visual areas of the inferior temporal cortex and the
pati& cortex have yet larger fields (for examples, see
[ 26,271).
There is, next, the question of complexity in the cellular
responses - itself a consequence of the enlargement of
receptive fields and the collecting of information from
large parts of the field of view. For example, the re-
sponses of cells in V4 correlate with the perception of
colours, whereas the responses of their counterparts in
~1 do not 1221; the generation of colour is itself a more
complex process than the registering of the presence and
intensity of different wavelengths [ 281, and to this extent
the responses of V4 cells are more complex than those
of Vl. Equally, the cells of area V5, or at least some of
them, respond to the coherent motion of an entire ob-
ject, whereas their counterparts in Vl (from which V5
receives its input) respond only to the components of
which the whole is made [29]. The consequence of
this is that the relevant cells of Vl may signal a direc-
tion of motion which is not identical to the direction of
motion of the entire object. But this complexity is not
a new departure; instead it is the continuation of a pro-
cess which starts in the retina itself, to the extent that the
photoreceptors have simpler receptive fields and simpler
responses than the ganglion cells into which they feed.
In a continuation of this process, the orientation selective
cells of Vl have more exigent requirements than the cells
of the lateral geniculate nucleus,
The effects of cortical lesions on vision
If, therefore, the anatomical and functional profile for the
prestriate cortex that we have built up over the past two
decades does not suggest a radical functional departure
from the kind of functional organization found in area
vl, is there any plausible reason to suppose that seeing
is vested in Vl and understanding in the surrounding cor-
tex, apart from the fact that lesions in Vl lead to nearly
complete blindness, whereas those in visual association
cortex do not? Insights into this problem may be gained
by a renewed study of the effects of cortical lesions on
vision. I do not refer here to the carefully controlled
experimental lesions in monkeys, which have been the
single worst guide to the organization of the visual cor-
tex imaginable, but to the natural uncontrolled lesions
in human brains produced by gunshot wounds or cere-
bral accidents which, paradoxically, have been a lot more
informative.
That lesions in Vl, and possibly also V2 (see [30] ),
should cause a total blindness is relatively easy to ex-
plain - such lesions do not usually spare a given sub-
compartment, for example, the blobs of Vl or the thin
stripes of V2 in which cells concerned with colour are
concentrated, but instead involve all compartments, The
consequence is that cells dealing with all the attributes
The visual association cortex Zeki 157
of vision are destroyed, leading to blindness. Naturally,
much the same thing would happen if all the specialized
visual areas were to be destroyed. But this could only be
the consequence of a lesion that is so large that it would
amount to an hemispherectomy, assuming it not to have
led to death.
The consequence of the more common type of lesion,
one restricted to one of the specialized visual areas,
is a blindness for the corresponding visual attribute. A
striking example is provided by the syndrome of cere-
bral achromatopsia, or acquired cortical colour blindness
following lesions in area V4, which is located in the fusi-
form gyrus (for a review, see [31]). No less specific is
the syndrome of cerebral akinetopsia or motion imper-
ception [17]. This is the consequence of lesions in area
V5 [32], which is located laterally and ventrally in man
and, perhaps surprisingly, in a zone (Feld 16) that Flech-
sig considered to have been myelinated at birth and
therefore a primordial area. But is the consequence of
such lesions a radically new kind of syndrome, con-
cerned with ‘understanding’ motion or colour, or is it,
as the physiology suggests, a more complex example of
the same phenomenon? Can meaning and understanding
be attached to vision only through the participation of the
visual areas of prestriate cortex, or can areas Vl and V2
contribute explicitly to both seeing and understanding
the visual world?
Examination of the so-called agnosic patients, as well as
patients with akinetopsia and achromatopsia, leads one
to a general theory of residual vision [6]. This sup-
poses that each visual area contributes explicitly to vi-
sual perception (that is in a way that requires no further
processing) and that the patient is able to see and to un-
derstand in exact relationship to that contribution and
no more. Moreover, the theory supposes that the ability
to see a particular visual attribute, for example motion,
is not dependent upon the integrity of the entire visual
pathway, up to V5 and possibly beyond. Instead, it sup-
poses that, if the latter is destroyed, the patient will be
able to see visual motion in proportion to the direct
and explicit contribution to vision that the intact parts
of the system, including areas Vl and V2 which feed V5,
are able to make. When area V5 is destroyed in an akine-
topsic patient, the directionally selective cells of area Vl
that feed it are not; consequently, the patient is aware
of the presence of motion but cannot make much of it
(see [33]). Equally, an achromatopsic patient is able to
discriminate between different wavelengths, but is unable
to combine this information to construct colours (see
[6] ), a deficit remarkably similar to the consequence
of lesions in macaque area Vd [34]. Indeed, the orien-
tation selective cells of Vl, which are able to respond to
pure chromatic borders [35,36], would endow an achro-
matopsic patient with an intact, or partially intact, Vl, with
the ability to detect the orientation of the boundary be-
tween two equiluminant surfaces of different colour, even
though the colours on either side of the boundary remain
identical to him [ 371,
Additional support for this view comes from comparing
the nature of the so-called agnosia in carbon monoxide
158 Cognitive neuroscience

patients, and in patients with large lesions in the prestri- Conclusion

ate cortex. It is almost certain that, in the former, area Vl
is much a&ted, although of course the areas of the pres- I have concentrated in this brief review on the conceptual
triate cortex are probably also compromised. The conse- doctrine that we have inherited about visual ‘association’
quence is a profound defect in form vision, with patients cortex, and hence about vision, and tried to show that
hardly able to recognize or copy simple geometric figures the separation between seeing and understanding what
such as triangles or squares [38]. The interpretation that is seen - a concept deeply tied to that of associa-
I have given to this syndrome is that even the elementary tion cortex - is not easy to achieve. One can make a
kind of integration and association which Vl is respon- fair argument - from ordinary visual perception, from
sible for - the generation of cells especially responsive anatomy and physiology, and from the study of the dam
to straight lines - becomes compromised. The nature of aged brain - that seeing and understanding are part of
the agnosia in patients with lesions in the prestriate cor- the same process, though no one would wish to deny
tex is markedly different. Now the patients can even draw that there are many instances in which we see things
complex figures, without being able to recognize the final that we do not properly understand. The concept of
product! Yet how is it that these patients draw? There is visual association cortex, in the sense intended by the
good agreement in the literature that the drawing is piece- early neurologists, is therefore perhaps now best aban-
meal, small segments of the picture, or of its outline - doned. But, in doing so, we must acknowledge that those
segments that the patient can see and understand - be- who originated the concept and speculated about it have
ing drawn, one after another. Once drawn, the patient can a high and honourable place in the history of our subject.
If the concepts that they fought for with such conviction
still only recognize small segments of his drawing and not
its entirety. It is the simple components of a figure that and passion have turned about to be false, we must re-
the patients are able to see and to understand because flect that the concepts that we today fight for, with no
less conviction and passion, may equally turn out to be
the integrative mechanisms necessary to construct simple
ilawed speculations in the vast ocean of the unknowns
forms, such as lines, are intact, while those needed for
that the visual brain still is.
more complex forms are compromised. The intact area
Vl makes a direct and explicit contribution to percep-
tion, but the destroyed prestriate areas are not able to
perform their function and hence associate the various
elements and organize into a larger whole. The patient References
consequently sees, understands, and is able to draw only
in proportion to what his intact Vl allows him to do. 1. FLECHSIG P: Developmental (Myelogenetic) Localisation of
the Cerebral Cortex in the Human Subject. Lancet lM1,
2:1027-1029.
2. FLECHSIG P: Gehirnphysiologie und Willenstbeorien. 1905.
Translated by Von Bonin G. In Some Papers on the Cerebral
Cortex, Fifth International Psychology Congress. Springfield,
Vl is as important for conscious experience Illinois: 1905: 73-89.

and understanding 3. LISSAUER H: Ein FaII von Seelenblindheit Nebst Einem

Beitrage zur Theorie Derseiben. Arch Pqhbtr Nervenkr
1890, 21:221-270.
There is, finally, the evidence from blindsight (for a re-
view, see [39]), when subjects blinded by lesions in area 4. CA~~PBELL AW: Histological Studies on the LocaIisation of
Cerebral Function. Cambridge: Cambridge University Press;
Vl are nevertheless able to discriminate some visual stim- 1905.
uli correctly, even though they commonly have no con-
5. Cm MH, BISHOP GH: Responses from an Association
scious awareness of having seen anything at all. It is very
Area Secondarily Activated from Optic Cortex. J Neuro
likely that when such blindsight subjects detect the di- physol 1954, 17~271-277.
rection of motion, signals relating to motion reach area
6. ZEKI S: A Vision of the Bruin. Oxford: Blackwell Scientific;
V5 directly, in the direct pathway from the lateral genicu- 1993.
late nucleus to V5 [40,41]. Direct physiological evidence
7. HUBEL DH, WIESEL TN: Receptive Fields, Binocular Interac-
has shown that cells in ~5 can maintain the property of
tion and Functional Architecture In the Cat’s Visual Cortex.
direction selectivity, although in a compromised state, af- J P@wol (Land) 1962, 160:106154.
ter ablation of V5. Yet the fact that blindsight patients
8. HUBEL DH, WIESEL TN: Receptive Fields and Functional Ar-
have no conscious awareness of the visual stimulus, and chitecture in Two Nonstriate Visual Areas (18 and 19) of
hence no understanding of it, suggests either that pre- the Cat. J Neurq0hyiol 1965, 28:229-289.
processing in Vl is a necessary step for stimulation to ZEKI SM: Functional Organization of a Visual Area in the
9.
gain consciousness, or else that it is necessary for the Posterior Bank of the Superior Temporal Sulcus of the Rhe-
operations performed by V5 to be referred back to Vl sus Monkey. J PLysiol (Land) 1974, 236:54’+573.
in the diffuse return projection linking V5 to Vl [42]. Of 10 ZEKI SM: Colour Coding in Rhesus Monkey Prestriate COr-
course, it is possible that both processes are necessary. tex. Brain Res 1973, 53~422-427.
Whatever the case, the results suggest that Vl is an essen- 11 ZEKI SM: The Functional Organization of Projections from
tial part of the process that allows conscious experience Striate to Prestriate Visual Cortex in the Rhesus Monkey.
and hence understanding of vision. Cold Smim Hat-b Ouant Biol 1975. 40:591a.
 The visual association cortex Zeki 159
-

12. Z,EKI S: The Distribution of Wavelength and Orientation Se- 28. IAND EH: The Retinex Theory of Colour Vision. Proc R
lective Cells in Different Areas of Monkey Visual Cortex. Instn Gt Br 1974, 47:23-25.
Proc R Sot Lond [Biol] 1983, 217:44+470.
29. MOVSHON JA, ADDLESON EH, Gtzt
MS, NEWSOME WT: The
13. DESIMONE R, SCHEIN SJ: Visual Properties of Neurons in Area Analysis of Moving Visual Patterns.
In Pattern Recognition
V4 of the Macaque: Sensitivity to Stimulus Form. J Neuro Mechanisms Edited by Chagas C, Gattass R, Gross CG. Pon-
pbysiol 1987, 57:835i868. tifical Academy: Citta de1 Vaticano; 1984: 117-151.

14. SCHE~N SJ, DESU~ONE R: Spectral Properties of V4 Neurons 30. HORTON JC, HOYT WF: Quadrantic Visual Field Defects.
in the Macaque. J Neurosci 1990, lo:33693389. Brain 1991, 114:1703-1718.

15. 2~x1 SM: Functional Specialization in the Visual Cortex of ZEKI S: A Century of Cerebral Achromatopsia Brain 1990,
31.
the Rhesus Monkey. Nature 1978, 274:423-428. 113:1721-1777.
16. ZEKI S, SHIPP S: The Functional Logic of Cortical Connec-
32. ZIHL J, VON CRAMON D, MAI N: Selective Disturbance of
tions. Nature 1988, 335:311-317.
Movement Vision after Bilateral Brain Damage. Brain 1983,
17. ZEKI S, WAIXON JDG, LUECK CJ, FR~STON KJ, KENNARD C, 106:313-340.
FRACKOWW( RSJ: A Direct Demonstration of Functional
Specialization in Human Visual Cortex. J Neurosci 1991, 33. HESS RH, BAKER CL, ZIHL J: The ‘Motion-Blind’ Patient:
11641-649. Low-Level Spatial and Temporal Filters. J Neurcuzi 1989,
9:1628-1640.
18. LMNGSTONE MS, H~REL DH: Anatomy and Physiology of a
Color System in the Primate Visual Cortex. J Neurosci 1984, 34. WALSH V, CARDEN D, BUTLER SR, KUUKOWSKI JJ: Tbe Effects of
4:30%356. V4 Lesions on the Visual Abilities of Macaques; Hue Dis-
crimination and Colour Constancy. Bebav Brain Res 1993,
19. POGGIO GF, GONZALEZ F, KRAUSE F: Stereoscopic Mechanisms in press.
in Monkey Visual Cortex, Binocular Correlation and Dispar-
ity Selectivity. J Neurosci 1988, 8:4531-4550. 35. Goup& P, KRUGER J: Responses of Cells in Foveaf Visual Cor-
tex of the Monkey to Pure Color Contrast. J Neur@ysiol
20. BA~ZER JS, RORINSON DL, Dow BM: Visual Responses of Area 1979, 42:850&O.
18 Neurons in Awake, Behaving Monkey. J Neuropbysiol
1977, 40:10241037. 36. THORELL LG, DEVAL~IS RL, ALBRECHT DG: Spatial Mapping of
Monkey Vl Cells with Pure Color and Luminance Stimuli.
21. ZEKI SM: Uniformity and Diversity of Structure and Function Vision Res 1984, 24:751l769.
in Rhesus Monkey Prestriate Cortex. J Pbysiol (‘Land) 1978,
2773273-2900. 37. HEY~~~D CA, Cowxu A, NEWCOMBE F: Chromatic Discrimi-
nation in a Cortically Colour Blind Observer. EurJ Neurosci
22. ZEKI S: Colour Coding in the Cerebral Cortex: the Reac-
1991, 3:802-812.
tion of Cells in Monkey Visual Cortex to Wavelengths and
Colours. Neuroscience 1983, 9:741-765. 38. HUMPHREYS GW, R~DWCH MJ: To See but Not to See. A Case
23. HUBEL DH, LMNGSTONE MS: Segregation of Form, Color and Study of Visual Aggnosia. Hillsdale, New Jersey: Erlbaum Asso-
Stereopsis in a Subregion of Priiate Area 18. J Neurosci ciates; 1987.
1987, 7:33783415. 39. WEISKRANTZ L: Blindsight. Oxford: Clarendon Press; 1986.
24. SHIPP S, ZEK~ S: Segregation of Pathways Leading from Area 40. YUKIE M, IWAI E: Direct Projection from the Dorsal Lateral
V2 to Areas V4 and V5 of Macaque Monkey Visual Cortex. Geniculate Nucleus to the Prestriate Cortex in Macaque
Nature 1985, 315~322-325.
Monkeys. J Comp Neural 1981, 201:81-97.
25. DE YOE EA, VAN ESSEN DC: Segregation of Efferent Connec-
41. FRIES W: The Projection from the Lateral Geniculate Nu-
tions and Receptive Field Properties in Visual Area V2 of
cleus to the Prestriate Cortex of the Macaque Monkey.
the Macaque. Nature 1985, 317:58-61.
Proc R Sot Lond {Biol] 1983, 21317380.
26. GROSS CG: Visual Functions of Infero-Temporal Cortex. In
Handbook of Sensory P&siology, vol 7, pan 3. Edited by Jung 42. SHIPP S, ZEKI S: The Organization of Connections Between
R. Berlin: Springer; 1972. Areas V5 and Vl in Macaque Monkey Visual Cortex. Eur
J Neurosci 1989, 1:30’+332.
27. MOUNTCASTLE VB, MOLTER BC, STEINMETZ MA, DUFN CJ: Look-
ing and Seeing. The Visual Functions of the Parietal Lobe. In
Dynamic RFpects of Neocortical Function. Edited by Edeiman S Zeki, Department of Anatomy and Developmentai Biology, University
GM, Gall WE, Cowan WM. New York: Wiley; 1984: 159194. College London, Gower Street, London, WClE GBT, UK.