Book review
Brain (2005), 128, 1226–1229
Measuring sight by sound
In proposing a vote of thanks for the three Special University
Lectures in Physiology that David Hubel delivered at University College, London, in February 1965, the late Professor
Joseph Barcroft said that they belonged in the same league
as those he had been privileged to have heard from Ramon
y Cajal, Sir Charles Sherrington, Lord Adrian and Sir John
Eccles, each one of whom had given major insights into the
nervous system. The accolade was nothing if not deserved. The
lectures were brilliantly delivered, and remain in my memory
as amongst the finest that I have heard on any subject. They
described the work that David Hubel and Torsten Wiesel had
begun in 1958, a collaboration that was to last for 25 years and
to revolutionize our knowledge of the workings of the visual
brain. Brain and Visual Perception is a record of that collaboration, most of it in the form of collected papers, with a foreword and afterword to each. Although almost all of the latter are
written by David Hubel, each author has contributed an autobiographical article. The entire book is an inspiration to read.
The original papers and the additional chapters are beautifully
written—which means that they are stylistically elegant, free
from jargon and cliché and, above all, devoid of the current,
vulgar, craze for acronyms and abbreviations and of other
devices that serve to make science even more inaccessible.
In fact, a re-reading of these papers in the chronological
order in which they are presented here serves to correct the
impression given by the authors that their work was nothing
more than a sort of fact-finding mission, devoid of any hypothesis. For, collectively, they give a powerful sense of the
logical development of work that culminated in a detailed
understanding of the functions and functioning of area 17 of
the visual cortex.
When the authors began their work on the visual cortex, and
more specifically on the primary visual cortex or area V1 (also
known as the striate cortex or area 17), not a great deal was
known. The visual cortex had been established as the recipient
of fibres from the retinas through the optic radiation. The work
of Salomon Henschen in Sweden, Tatsuji Inouye in Japan and
Sir Gordon Holmes in England had established that there is a
topographic map of the retina, and hence of the visual field,
within V1 which, in the mid-twentieth century, was considered
to be the sole visual area in the brain. By the time their collaboration was finished, Hubel and Wiesel had shown that the
ordering of V1 is much more precise and elegant; they had
demonstrated the presence and shape of ocular dominance and
orientation columns within it; established the details of connections between the geniculate nucleus and V1; and asked
daring questions about the role that nature and nurture play in
its development. Their work on V1 also led them to develop
what has come to be known as the hierarchical model of visual
BRAIN AND VISUAL
PERCEPTION
The story of a
25-year collaboration
By David H. Hubel
and Torsten N. Wiesel
2004. New York:
Oxford University Press.
Price £29.99
ISBN 0-19-517618-9
perception, which supposes that the same details of the visual
world are reanalysed at increasing levels of complexity. In
this, they were substantially wrong, since it is now generally
agreed that the simultaneous, parallel, processing of different
attributes of the visual world is the modus operandi of the
visual brain although a hierarchical strategy may characterize
each of the parallel systems. Read today, some 50 years after
the initial work was published, the papers still retain their
freshness and their capacity to arouse wonder, not only at
the way in which nature has elaborated such an impressive
organ, but also at the tenacity and the powerful conceptual
thinking that was behind their collected work.
Several factors went into making this collaboration one of
the most outstanding in neuroscience. There was, of course, the
element of chance behind many of the great leaps that came
from their collaboration, starting with the fact that both happened to be in Steve Kuffler’s laboratory at Johns Hopkins.
The epoch-making discovery of orientation-selective cells in
the cortex was itself a chance occurrence, arising from the
fortuitous insertion of a slide into the projector. The imaginative work that led to a direct anatomical demonstration of
ocular dominance columns in the striate cortex was made possible because Janet Chen, an expert histology technician, had
by chance moved to Boston; the failure to notice any distribution of autoradiographic material in striate cortex after eye
injections was corrected when a chance visit to Ray Guillery
alerted Hubel to the fact that its distribution is best viewed in
dark-field illumination. But chance was merely a catalyst, and
to them it was ‘more a matter of bull-headed persistence, a
refusal to give up when we seemed to be getting nowhere’. The
truth—which they themselves cannot utter—is that what distinguished their work from that of others was a conceptual
# The Author (2005). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oupjournals.org
Book review
David H. Hubel
Torsten N. Wiesel
brilliance; and with that kind of intuitive brilliance fancy
methodology was unnecessary. Before Hubel and Wiesel
started their work, most believed that the visual cortex
would be activated by light, as such. Failure to achieve results
with diffuse light stimulation was a trigger for the construction
of more sophisticated apparatus. In Germany, Richard Jung
and his colleagues spent much time and effort constructing
‘elaborate machines’ to activate the cells with diffuse light.
Jung was later to recount that he might have discovered the
orientation-selective cells during his 5 years’ work on the
visual cortex if he had used a stick ‘instead of the quantifying
machine’. Hubel and Wiesel had themselves used a now
outmoded approach to stimulate the visual system, when
that chance insertion of a slide into the projector elicited a
wild response from a cell. Their concern from then on was
to simplify the machinery and make the cells a good deal easier
to study. For them, ‘just as important as stubbornness, in getting
results, was almost certainly the simplicity, the looseness, of
our methods of stimulation. The incredible crudeness of our
first slide projectors . . . and our refusal to waste time bothering
with measuring intensities, rates of movement and so on . . . all
worked in our favor’. The term ‘loose’ is curiously out of
place, given how much valuable information was obtained
with it, and how little from sophisticated stimuli. From then
on they seemed to have developed a lasting contempt for fancy
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machinery, Hubel once boasting that the best use they could
make of their computer was to heat the laboratory. How could
one avoid this disdain when papers, published as late as 1977,
using sophisticated methodology and advanced computer
analysis, did not improve much on the precision with which
the properties of cells were described, and provided no
new insights whatsoever? How can one admire the detailed
and tedious measurement of the orientational preferences of
cells that are not orientation-selective, as some have tried to do
with the directionally selective cells of V5?
There is perhaps a little overmodesty in the description of
their work as being hypothesis-free, or what many would today
describe pejoratively as a sort of fishing expedition. Even if
true, this was a major fishing expedition with an ineluctable
and beautifully exploited logic; and the catch was astonishing.
It is no wonder that every chance was seized avidly. Once
orientation-selective cells were discovered (by chance) in
the visual cortex of an animal (the cat) which has two eyes
and a retinotopically organized primary visual cortex, the rest
followed easily, or so this collection of papers makes it seem.
The succession of questions can be summarized as follows:
How many orientations are represented within any given
retinotopically defined position of the visual field? How are
cells responding to different orientations organized with
respect to one another? Are all orientations represented for
each eye? How are the orientation columns and the ocular
dominance columns organized with respect to each other?
What is the overall organization of the two sets of columns
in the context of the topographic map within V1? Given that
visual deprivation early in life leads to lifelong blindness—a
topic widely discussed since the time of John Locke but put on a
scientific and clinical basis by the publication of Marius von
Senden’s book Space and Sight (1962)—it was natural to want
to study the effects of visual deprivation on the specificity of
visual cells in the cortex. Here, two eyes were better than one,
since it was possible to deprive one eye, or both, or neither. It
would, of course, be stretching things too much to claim that the
decision to work on a two-eyed animal was taken by chance
but, even if this accident is allowed, they still used the two eyes
in a most imaginative way. Buried within this set of questions is
some kind of implicit hypothesis. And the authors were well
aware, right from the start, that their undertaking was a major
one and that they were on to some striking findings. Why else,
as they tell us, would they project to write a book as early as the
1960s, well before their work came to maturity? Why else,
too, would they have been so aware of potential competitors,
jealously guarding their results and projected experiments?
It is likely that their apprenticeship prepared Hubel and
Wiesel, if not for the accidents and lucky breaks, then at
least for how to proceed once the significance of the accident
had been appreciated. The biographical sketches detail their
brilliant intellectual surroundings. The catalogue of names is a
veritable aristocratic roll call: Bernard Katz, William Rushton,
E. D. Adrian, John Eccles, Alan Hodgkin, Andrew Huxley,
Edwin Land, Michael Fuortes and Francis Crick. Indeed they
regard themselves as the scientific great-grandsons of Charles
1228
Book review
Sherrington, a lineage of which the latter would no doubt
have approved. No room here for the more modest in ability,
who might nevertheless come up with an interesting question
or two. Towering above all in inspiration to them was Steve
Kuffler, the grand maestro of neurobiology in the 1950s and the
1960s, who had surrounded himself with brilliant investigators. Clearly, the atmosphere at Johns Hopkins, and later at
Harvard Medical School, was highly congenial and deeply
inspiring. Clearly, too, the focus was on the problem rather
than on thoughtless measurement. Hubel recounts how he was
once advised by Kuffler to stick in some quantification, so as
to soothe the scientific conscience of the mindless measurers,
making the paper seem more scientific and therefore better
suited for publication. He laments that their work would be
unpublishable today, since referees, under the guise of a
scientific rigour that is both coarse and imperceptive, would
demand a host of detailed measurements. In one paper, they
write of the long time taken to produce a graph using a computer, adding: ‘We concluded that for both speed and for precision it is hard to beat judgments based on the human ear.
Certainly [the curves] could not have been obtained with computer averaging methods before the authors reached the age
of mandatory retirement’. It is difficult to deny that their work
would have suffered greatly if they had been working in the
present era of white-coated, rubber-gloved and dispassionate
scientific honesty, one that, distrustful of human judgement,
confides all measurements to a computer that supposedly
does not suffer from human bias. Yet it is also interesting
and instructive to compare the results that Hubel and Wiesel
obtained when they judged the response specificities of cells by
ear (itself not a negligible measuring device) with the host of
papers that make generous use of the apparently neutral
computer-generated ‘orientation selectivity index’, the ‘colour
selectivity index’, and many other indices. After a quarter of a
century of rigorous application, the latter have revealed nothing or little that is interesting or new. The authors themselves
make the point, perhaps unwittingly, in the commentaries that
follow each paper. Advances there have been, they seem to be
saying, but nothing to compare with the original discoveries.
It is, no doubt, this poverty of results, compared to the richness of the original findings, that has led David Hubel to regard
modern technologies, and the mathematical pitchforks associated with them, with such disdain. The Epilogue of the book
has him wandering sadly through the debris left by the muchvaunted computational approach which, one cannot but agree,
has contributed little that is of importance to understanding
how the brain works. He disapproves, as indeed do I, of linear
systems analysis and apparently shares my horror for the
current craze for ‘multiplexing’, the belief that few if any
cells in the visual brain are highly specialized and that most
of them are multipurpose. He has nothing but praise for the fact
that the major textbook of molecular biology, The Molecular
Biology of the Gene, contains no equations and that ‘no one has
tried to fit a protein molecule to a Gabor function’. Before
anyone dismisses these views too hastily, it is worth considering how much information the ‘crude’ techniques used
by Hubel and Wiesel gave, and how little, by contrast, these
fancy approaches have provided. The evidence is all there in
this book.
How did such a collaboration last for so many years and
why did it eventually end? The first question is relatively easy
to answer. One successful set of experiments led to another,
generating an unstoppable momentum. Both authors were
intoxicated enough by their results to persevere with one
experiment and then plan and push on with the next. Several
factors aided them in this. Steve Kuffler was evidently some
kind of Lorenzo de’ Medici, content to see brilliant work
progress in his department, dispensing advice in an avuncular
way and not anxious, as so many are today, to add his name
to the papers and thus get his cut of the glory. The relationships
established in the laboratory were evidently friendly enough
for the authors to say nothing more than that they were ‘sometimes mixed with resentments and varieties of complexes’.
Crucially, both were spared the curse of administration—
one that so many academics, in spite of their protestations,
love. After one year administering the Physiology Department
at Harvard, Hubel had had more than he could take when
the installation of a pencil sharpener necessitated at least
two elaborate meetings. They were also working at a time
when cats were even more plentiful than monkeys and not
much more expensive. Editors were more relaxed and referees
kinder. Nor were the grant-giving committees quite as forbidding as today. The authors state that their kind of work
could not be done today. Sadly, they are right. Their laboratory,
small in size and shared with others, encouraged continual
dialogue and discussion—one of the characteristics of great
laboratories such as the Laboratory of Molecular Biology in
Cambridge, UK, or the Bell Laboratories, USA. One gets the
impression that there was also a feeling of self-sufficiency. One
of the authors’ great strengths—but in the longer term also a
weakness—was their understandable indifference to work
done by others, perhaps encouraged by Steve Kuffler’s oftrepeated question: ‘Do you want to be a consumer or a producer?’ For example, even in this book, and after so many years of
discussion, they still believe, erroneously, that I mapped area
V5 of the owl monkey in 1980, thus getting both the species and
the date wrong, though I should be grateful that they got my
name right! They are not even aware of where V5 is, describing
it as lying in the ‘anterior lunate sulcus’, whereas it is actually
located some distance away, in the posterior bank of the
superior temporal sulcus. This is surprising, since V5 is now
one of the most studied visual areas after V1 and is coming
close to surpassing the latter. But all this presumably matters
little to David Hubel and Torsten Wiesel, since the work was
not undertaken by them! It is said that on one occasion, when
asked whether he intended to respond to criticisms made of
their work in a paper, Hubel replied that, to do so, he would have
to read the paper, which was more than he was prepared to do.
By the time they parted company in 1980, the authors had
succeeded in charting the anatomy and physiology of area V1
of the brain in greater detail than ever before, and making it
the best understood area of the cerebral cortex. They had used
Book review
almost all techniques available to them; charted ocular
dominance and orientation columns and looked at their anatomy; established with greater precision than ever before the
details of how the fibres from the lateral geniculate nucleus
terminate in the visual cortex; established the concept of the
column in the visual cortex firmly; shown that selectivities are
established at birth and are susceptible during a critical period
after that; and, above all, with their ‘loose’ methods had introduced new and very high standards of evidence into cortical
neurobiology which few have managed to emulate. Why, then,
did this flourishing scientific collaboration end? Their work
had been mainly on area V1, or area 17, and with so much
achieved it seemed as if V1 was well enough understood, and
the work thus began to run out of steam. Indeed, as early as 1968
they had thought of V1 as sufficiently well characterized that
‘despite the large areas still unexplored, in broad outline the
function of area 17 is probably now relatively well understood’.
It was to areas beyond V1 that one should turn one’s attention,
or so they implied when they wrote in the same paper ‘How this
information [in area 17] is used at later stages in the visual path
is far from clear, and represents one of the most tantalizing
problems for the future’.
In his autobiographical sketch, Torsten Wiesel writes with
disarming honesty that ‘there may have been a more profound
reason that our partnership came to an end. The additional
demands on our time [came] when we were investigating
the properties of cells of higher visual areas beyond the primary visual cortex, an exploration that each of us eventually
regarded as a failure . . . The two naturalists, who for so
long had journeyed together with a seemingly inexhaustible
sense of wonder, were unaccustomed to the frustrations that
are the daily bread of so much scientific research . . . what
developed between us, our special bond and private dialogues,
took place while we carried out our experiments. When these
explorations stalled, when the wonder faded, so did our collaboration. Perhaps it was necessary for each of us to turn to
new partners and questions’.
It is indeed through the exploration of the higher visual areas
that their concept of hierarchy began to be questioned.
That concept was largely the result of concentrating on
1229
orientation-selective cells and ignoring other categories of
cell. They managed to identify different levels of complexity
in the functional properties of orientation-selective cells, and it
is this that led them to the hierarchical concept of visual physiology. Ironically, it was adherence to this hierarchical doctrine
that made them misinterpret, or not interpret, the functions of a
visual area in the cat that is equivalent to area V5 in the monkey,
the Clare–Bishop area, in an article that they describe as ‘not
one of our favorite papers’. Hubel was later to repudiate this
exclusive hierarchical concept implicitly, but never explicitly.
The implicit repudiation came with the work he did with
Margaret Livingstone, which showed that their earlier model
of V1 was incorrect; that there was a functional segregation
within V1, much as had been predicted from the demonstration
of functional specialization among the higher visual areas of
the brain, beyond V1, and which receive their input from V1.
It is a pity that Hubel and Wiesel ignored the concepts of
functional specialization and parallelism, established by work
in the higher visual areas. It is a pity, too, that in gazing into the
future through the past David Hubel (the main author of the
commentaries of this book) has nothing to say about this
functional specialization—perhaps because it does not figure
in their collaboration. It is, in my view, a major oversight, but
it is an oversight that one might want to forgive, much as
one would forgive Einstein for reputedly ignoring quantum
mechanics. When one has finished rereading, or reading for
the first time, the extraordinary output that has resulted from
this legendary collaboration, one decides pretty much to
forgive such blemishes. Neuroscience should rejoice that,
during a mere 25 years, its world was enriched not only by
a wealth of knowledge but also by new standards of evidence
and elegance of methodology which have left a permanent
imprint.
Semir Zeki
Laboratory of Neurobiology
University College London
London, UK
doi:10.1093/brain/awh507