Pergamon

PII:S0893-6080(96)00020-2

Neural Networks, Vol. 9, No. 4, pp. 72%729, 1996 Copyright © 1996 Elsevier Science Ltd. All rights reserved

Printed in Great Britain 0893-6080/96 $15.00 + .00

B O O K R E V I E W

A Vision of the Brain By Semir Zeki , Blackwel l Scientific Pub l ica t ions ,

Oxford : 1993, 366 pp. , I S B N 0-632-03054-2

Semir Zeki's magnum opus on visual neurophysiology, A vision o f the brain (Blackwelt, 1993) is destined to become a classic, both for its readability and its innovative content. The central question of the book is the age-old problem of how does the brain/mind represent the world? Zeki attacks the question using a scientific rather than a philosophical approach. Yet he manages to weave together critical discussions of history, neuroanatomy, and physiology, and even philosophy. The selection of illustrations is first- rate. The figures showing different brain regions at multiple scales are especially informative. For the student and for researchers in psychology, computer science, and related fields who are not neuroscientists, Zeki also gives numerous examples of how to think about neuroscience. He includes useful discussions of many of the techniques used by neuroscientists including various staining methods and current functional imaging techniques.

Zeki's story begins at the turn of the eighteenth century with Thomas Young's (1802) description of the trichro- matic theory of color vision. Already in the first chapter he begins his personal criticism of the history of neuroscience, using subheadings such as "Neurologists adopt a simplistic view of color vision". In his criticisms, his tone is often sarcastic: "The implications of Verrey's conclusions were momentous, indeed so momentous that even he failed to see them" (p. 34). Throughout the book he examines the interesting historical question of why early researchers "misinterpreted" much of the evidence available to them (a statement made possible with the hindsight provided by more recent data and theories), which Zeki claims should have been clear to all involved.

One fallacy of early neuroscience was to assume that because the different retinal receptors were differentially sensitive to the wavelength of light, and because those receptors had direct connections to the primary visual cortex, the sensation of color was in some real sense equivalent to the wavelength of the light reflected to the retina. A second error was the general acceptance of the view that all aspects of basic visual function were located within the same anatomical area (namely primary visual cortex). A related error was the notion that the basic process of "seeing" and the seemingly higher level process of "understanding" were functionally and anatomically distinct. Also, the relatively more recent notion that cortical processing operates in a linear hierarchical fashion, where basic elements analyzed at lower levels are used to construct

Acknowledgement: We would like to thank Paul Havig for his comments on an earlier draft of this review.

increasingly complex representations at higher levels, would also appear to be in need of modification. Unfortunately, many. of these early misconceptions have survived in some form to influence current views of brain function.

Some of these early views were understandable given the preponderance of the evidence. However, Zeki points out that there were also tell-tale clues that these early interpretations were not entirely accurate. Broca's (1861) discovery of a distinct cortical area for speech production made it plausible that vision should be anatomically localized as well. On the other hand, the evidence from Fritsch and Hitzig (circa 1870) on the localization of the motor system made it plausible that different sub-functions could be localized in different regions, since speech involves motor processing but is not localized in primary motor cortex. The discovery of achromatopsia, the inability to perceive color in a portion of the visual field, should have provided evidence for the functional and anatomical separation of color and form vision, yet the observation that achromatopsia was often accompanied by scotoma (a blindspot in the visual field), due to the (now known) fact that the cortical color area borders on the primary visual area, gave the false impression that the processes were co- localized.

To correct the flaws inherent in these early views and to provide a coherent description of vision and brain function based on current knowledge of anatomy and physiology is a central goal of the book. For example, color is not equivalent to wavelength, but is identified as the result of a complex comparison of wavelengths emanating from a range of locations across the visual field. In general, sensations (by which Zeki definitely means those percep- tual events of which we are conscious) are a complex construct only indirectly related to the physical stimuli which give rise to them. The notion that perceptual representations are constructions allows Zeki to argue convincingly on computational grounds that different visual functions (that is, the identification of different visual aspects---color, motion, etc.) must be separately localized because different functions are implemented with different algorithms and therefore cannot utilize the same neural circuitry. This implies that if what is meant by visual "understanding" is at least in part the identification of certain important invariant components of visual input (e.g., color and motion), then understanding is a necessary component of seeing itself and there are not separate locations devoted to the "registration" of basic visual primitives (indeed color and motion are not primitives in the usual sense, since they are constructs), on the one hand, and the combination or association of those primitives into a meaningful and coherent whole, on the other hand. Zeki treats the issue of perceptual integration more fully in the last few chapters of the book.

To support his view that neural (and, Zeki would say,

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therefore mental) representations are dynamic constructs designed to solve particular problems or extract particular information, Zeki must make modifications to a number of standard views on the organization of the brain. Many of the proposed innovations of his new "vision" are not original with Zeki, but he brings together in one place a discussion of many important issues. In a rapidly expanding field of study such as that of neuropsychology or cognitive neuroscience, which gives rise to an over- whelming number of diverse and fractionated presentations (e.g., see Gazzaniga, 1995), unifying discussions such as Zeki's are in great need.

The notion that visual information is processed hierarchically, from simple features to increasingly abstract representations, a notion which seemed to be supported early on by the work of Hubel and Wiesel (in the 1960s), is one of the standard doctrines in need of revision. Chapter 9 provides a clear and fair-handed treatment of Hubel and Wiesel's work. But again Zeki points out that different visual functions implement different algorithms and therefore require separate, parallel pathways. And this seems to be the case anatomically: " . . . the concept of hierarchy as an exclusive strategy had no solid foundations. It was sufficient to show that each of the specialized visual areas receives an independent input from V1 for it to collapse too" (p. 92).

The notion of "map", a standard phrase among physiologists, is one of the concepts that Zeki hopes to update. Typically cortical maps are thought of as static, generally spatially topographic representations of some aspect of the sensory world. Although many cortical representations may fit this standard description to some degree, many important visual processes cannot be captured in this fashion. For example, what does a "map" of surface color (as opposed to wavelength) look like? What does a "map" of object motion (where local and global dynamics may appear to contradict each other) look like? Many of the more complex cortical representations take the form not so much of "maps" but of representa- tions constructed from a variety of inputs. The fact that such higher-order representations change as a function of attention and other related processes means also that they are dynamic constructions from sensory input and not merely a one-to-one representation of what is happening at the retina.

No doctrine is sacred under Zeki's "reinventing" of the brain. Although of recent vintage, the "what and where" doctrine (e.g., Mischkin et al., 1983), the idea that location and form information are processed by separate neural pathways has taken on the status of accepted fact. But consistent with his constructionist view of neural repre- sentation, Zeki argues adamantly against the notion that form perception and location perception are distinct processes: "Perhaps a far better way to look at this system is to accept that each area will draw on any source to undertake its specialized task. Examples of one source of information providing material for another are common. Shape can be derived from shading; depth can be derived from motion. The precise position of an object and its relationship to other objects (spatial vision) can give the vital clue to the identity of the object, and the precise shape of an object can give the vital clue to its position . . . There

are, in brief, far too many facts militating against the "what and where" doctrine for it to be retained a serious indicator of how the visual cortex is organized" (p. 194).

Chapter 21, "The modularity of the brain" is a crucial point in the development of Zeki's vision of the brain. Again, he qualifies his use of the term "module": " . . . while there is no doubt that the cerebral cortex is modular in its organization in the sense that, even for a given modality, it assigns geographically separate cortical areas and sub- regions of areas to different specializations, we still have no agreement as to whether there is a unit of organization which is repetitive, and the same everywhere in the cortex, and which we can think of as the cortical module" (p. 202).

He does however propose a set of general rules which seem to apply to the cortex as a whole. First, all cortical areas have both inputs and outputs, implying " . . . there is no cortical terminus, no final destination where the soul or consciousness, for example, may reside" (p. 203). This is in agreement with certain contemporary philosophical ap- proaches (e.g., Daniel Dennett's) to the problems raised by Cartesian views of consciousness. Second, each cortical area (or zone) both sends and receives connections to and from multiple other cortical areas. This means that each area is involved in more than a single computation and furthermore that the results of different computations are important to more than one cortical area. He coins the term "operational connection" to refer to this second regularity. The term "topographic connection" refers to projections between cortical areas that have a roughly point to point correspondence. These kinds of connections are of course necessary for maintaining the integrity of spatial maps. However, it would seem to be the case that it is often necessary for more abstract information to be commu- nicated from one cortical area to another. In this case, operational connections where the inputs arise from numerous cells within a cortical area, are integrated within the area, and then projected to specific sub-regions of other areas, are necessary. Third, all cortical areas project to subcortical areas, and it is usually the case that the cells projecting to subcortex are not the same as those projecting to other cortical areas. This is additional evidence that each brain region is engaged in multiple operations.

Chapters 23-26 provide an excellent description of the computational and neural mechanisms of color vision. One of Zeki's conclusions is that a given color is not so much an attribute as a category, that is, color is the invariant element resulting from a complex process of comparing the pattern of relative intensities of different wavelengths of light reflected from a large portion of the visual scene. This leads to the potentially far reaching suggestion that the cortex itself can be viewed as a categorizer. Although Zeki himself does not emphasize the possibility, his suggestion implies the profound notion that a correct theory of color vision could well provide the groundwork for a general theory of categorization.

The book ends with a discussion of sensory integration. If different visual functions are performed in parallel cortical pathways, one may ask what mechanisms exist for integrating the different processes. Although he pays some service to the currently popular notion that synchronized neural oscillations may play a role in the integration process, Zeki emphasizes that perceptual

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information is integrated as a consequence of the way cortical areas are interconnected. The fact that so-called higher level cortical areas always reciprocally connect to so- called lower order areas (feedback or "re-entry") ensures that the computations performed at various stages of perceptual processing are not performed in isolation. A cortical area performing a particular computation or implementing a particular algorithm always (or almost always) sends the results of its labors back to the area in which the information originated. The existence of feed- back helps to solve a number of problems that face a computational system as complex as the visual system. As neural receptive fields become more complex, they increase in size and lose spatial precision. This makes sense, since neurons with complex receptive fields are engaged in operations which need to be spatially invariant. However, feedback connections to areas which have precise spatial maps, allow the spatial detail lost at the higher level to be recovered. Furthermore, feedback is necessary to overcome disagreements between local, low level computations and global, high-level computations. An example of such conflict occurs in motion perception, where globally an object is perceived to move in a single direction, but very locally, the parts of the object may be seen to move in different directions. In the case of a single diamond moving to the right, each component line, viewed in isolation, will be perceived as moving diagonally in different directions. Zeki proposes that re-entry serves to resolve the differing representations.

Zeki himself certainly takes a negative view of current work in computational neuroscience and neural network modeling. He maintains that much modeling is done that fails to take into account what is known about the actual workings of the brain. Ironically, his representative computational neuroscientist is David Marr, a researcher known for his efforts to combine knowledge from the computational and physiological domains. Marr was certainly a leader of the field in his time; however, because his physiologically based work focussed primarily on problems of "early vision" and because of recent anatomical, physiological, and computational advances, his work does not adequately represent the variety and

sophistication of the work being done by current modelers. Regardless of the validity of Zeki's criticisms, it is clear that computational and experimental neuroscientists have a great deal to learn from each other, and that the interdisciplinary approach to neuroscience that Zeki so strongly advocates elsewhere in his book is the most fruitful route to follow. With this in mind, there is a great deal in Zeki 's book that is of interest to neural modelers.

To sum up, A vision of the brain is an outstanding work. It is well-written and fun to read. For those just beginning to study the complex workings of the brain, one can hardly do better than to learn from one of the leaders in the field. For psychologists, computer scientists, philosophers and others who are not experts in phsysiology, as well as neuroscientists who are not experts in visual neurophysiol- ogy, Zeki 's review and synthesis will prove informative and enlightening. Although experts in the field may find some of the details repetitive, Zeki's arguments about history and philosophy are sure to stir some interest, if not controversy, and his overall framework provides refreshing insight into the workings of the brain, which Zeki himself emphasizes, we are only beginning to understand.

Vincent Brown Department of Psychology

University of Texas at Arlington Arlington, TX 76019

U.S.A.

Bruno Breitmeyer Department of Psychology

University of Houston Houston, TX 77004

U.S.A.

REFERENCES

Gazzaniga, M. S. (Ed.) (1995). The cognitive neurosciences. Cambridge, MA: MIT Press.

Mishkin, M., Ungerleider, L. G., & Macko, K. A. (1983). Object vision and spatial vision: Two cortical pathways. Trends in Neurosciences, 6, 414-417.