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PERSPECTIVES
Chester,Nova Scotia in Canada. As a child he
was a precocious and voracious reader.When
he was 16,the family moved to Dartmouth,
Nova Scotia, and the following year, Hebb
entered the Faculty of Arts at Dalhousie
University in Halifax
(FIG. 2).He majored
in English with the intention of becoming a
novelist
8
.Hebb graduated with a B.A. in 1925
and taught at his old school in Chester for a
year. This was not a success, and his novel
writing did not progress.
Hebb spent the next year harvesting on
a farm in Alberta, labouring in Quebec,
and reading Sigmund Freud. This made him
consider a career in psychology and he
approached the chairman of the McGill
University Department of Psychology,W.D.
Tait, about doing graduate work. He was
given a reading list and told to come back
next year. To earn a living, he resumed
his career as a schoolteacher.The following
year (1928),he was accepted as a part-time
graduate student at McGill. He was also
appointed principal (headmaster) of a school
in a working class suburb of Montreal,where
there was a high rate of absenteeism and
drop-out.With the help of two psychology
professors,Kellogg and Clarke,from McGill
University, he improved the situation by per-
suading the children that school-work was a
privilege, giving the children more interesting
things to do in class and sending any who
disrupted the class outside to play
9
.
In 1931, Hebb was bedridden with a
tubercular infection of the hip.During that
time,he studied Sherrington’s The Integrative
Action of the Nervous System
10
and Pavlov’s
Conditioned Reflexes
11
,which had been pub-
lished in English in 1927, and he wrote a
theoretical M.A.thesis entitled Conditioned
and Unconditioned Reflexes and Inhibition
12
.
The thesis is of interest because it contains
the seed of what was to become known as the
Hebb synapse (
BOX 1 and BOX 2).The thesis
was passed cum laude by two examiners, one
of whom was Boris P. Babkin, who had
worked with Pavlov in St.Petersburg and Hill
in London,and who,after a brief period at
Dalhousie University, joined the Physiology
Department at McGill.Babkin arranged for
Hebb to conduct research on Pavlovian con-
ditioning with Leonid Andreyev, who had
also come from Pavlov’s laboratory to pursue
his research at McGill.
During 1933–1934, Hebb wrote an unpub-
lished booklet entitled Scientific Method
in Psychology: A Theory of Epistemology Based
on Objective Psychology (Hebb,D.O.,unpub-
lished observations). Many of the ideas in it
were later incorporated into The Organization
of Behavior and Essay on Mind
13
. But by
January 1934, Hebb had become disillusioned
both with Montreal and McGill. His wife had
died on his twenty-ninth birthday, after a car
accident. Furthermore, his school reform
experiment was, in his words,“defeated by the
rigidity of the curriculum in Quebec’s protes-
tant schools”
8
.As for his graduate studies
at McGill, most of the psychology faculty
was engaged in educational psychology
and intelligence testing,whereas Hebb was
becoming increasingly interested in physio-
logical psychology. He did not consider the
Pavlovian conditioning experiments he was
conducting to be true physiological psycho-
logy, and he was critical ofthe methodology.
Ph.D. research with Karl Lashley
Having decided to leave Montreal,Hebb wrote
to Robert Yerkes at Yale, and was offered a posi-
tion to study for a Ph.D. Babkin, however,
urged him to apply to Lashley if he wanted
to learn about physiological psychology,
and in July 1934 Lashley accepted Hebb to
work with him at the University of Chicago
14
.
Neuroscientists associate the name of
Donald O. Hebb with the Hebbian synapse
and the Hebbian learning rule, which underlie
connectionist theories and synaptic plasticity,
but Hebb’s work has also influenced
developmental psychology, neuropsychology,
perception and the study of emotions, as well
as learning and memory. Here, we review the
work of Hebb and its lasting influence on
neuroscience in honour of the 2004
centenary of his birth.
Donald O. Hebb (FIG. 1) is best known for
his neurophysiological postulate on learning
(
BOX 1,BOX2 and BOX3), which appeared in his
book The Organization of Behavior
1
,published
in 1949. Stemming from the postulate,
Hebb’s name is increasingly used as an adjec-
tive, so that we have the Hebb synapse,
Hebbian synaptic plasticity, Hebbian learning
rules, Hebbian neural networks and even
anti-Hebbian learning.The postulate forms
part of Hebb’s neural theory of perception,
and much of our current understanding of
functional neural connections is based on
Hebbian concepts
2,3
.His book also contributed
to many aspects of human neuropsychology,
developmental psychobiology and cognitive
neuroscience
4–7
.In this article, we trace the
path that led Hebb to develop the theory that
he presented and explored in The Organization
of Behavior,and elaborate on the influence it
has had on psychology and neuroscience.
Hebb’s student years
Hebb’s parents were both country physicians,
and he was born in 1904 in the town of
NATURE REVIEWS | NEUROSCIENCE VOLUME 4 | DECEMBER 2003 | 1013
The legacy of Donald O.Hebb:
more than the Hebb Synapse
Richard E. Brown and Peter M. Milner
TIMELINE
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PERSPECTIVES
psychology at Radcliffe College, for E. G.
Boring. He published his Ph.D. research
15
and
completed the research that he had started in
Chicago
16
.Informal discussions with Lashley
and the members ofhis laboratory helped him
to complete his psychological education.
Neuropsychology at the MNI
In the summer of 1937, Hebb’s sister Catherine,
then a Ph.D. student with Babkin at McGill
University, told him that Wilder Penfield,
founder ofthe Montreal Neurological Institute
(MNI),was looking for someone to study the
psychological effects of brain operations.Hebb,
newly married to his second wife Elizabeth,
applied for the job and was appointed a fellow
ofthe MNI. Hebb’s work in Penfield’s surgery
marked a turning point in the scientific study
ofhuman neuropsychology.Hebb was critical
ofboth the Stanford Binet and the Wechsler
intelligence scales for use with patients
17,18
.
He observed that lesions of different brain
areas produce different cognitive impairments,
and he suggested that,rather than measuring
overall intellectual change,one should seek
specific aspects of intelligence that were
affected by a brain lesion
19
.
Hebb therefore assembled a battery of
tests, including two new tests — the verbal
Adult Comprehension Test and the non-
verbal Picture Anomaly Test — which he was
developing with N.W. Morton of the McGill
Psychology Department
20
.Using the Picture
Anomaly Test, he provided the first indication
that the right temporal lobe was involved in
visual recognition
17
.His most important
papers from this period were those concerning
but Hebb had to change his research topic.In
Spring 1936, Hebb submitted a thesis on the
vision of rats reared in darkness, and he
received a Harvard Ph.D. For the next year,
Hebb worked as a research assistant for Lashley,
and also as a teaching assistant in introductory
Hebb’s Ph.D.thesis topic was ‘The problem of
spatial orientation and place learning’, but
before he had completed the research,Lashley
accepted a position at Harvard.Hebb and two
ofhis fellow students, Beach and Smith,were
accepted as Ph.D. students at Harvard in 1935,
Hebb is born
in Chester,
Nova Scotia
on 22 July.
Accepted as a part-time graduate
student in psychology at McGill University
in September 1928. Starts his ‘learning
as a reward’ strategy in an elementary
school. From 1930 to 1931, he is
bedridden for a year with a tubercular hip.
He writes his M.A. thesis in bed and
submits it in April 1932.
Enters Dalhousie University in 1921. Graduates
with a B.A. in English in May 1925. Teaches in
Chester, Nova Scotia from 1925 to 1926. Works
on a farm in Alberta during the summer of 1926.
Spends winter in Quebec as a labourer and
reads Freud. Meets W. D. Tait at McGill
University, who sends him to read James and
Ladd & Woodworth. In Autumn 1927, he
becomes a schoolteacher in Montreal.
Decides to study physiological
psychology, and works with Lashley
in Chicago for three academic terms.
Moves to Harvard with Lashley in
September 1935, and submits
Ph.D. thesis in March 1936. From
1936 to 1937, he works with Lashley
and E. G. Boring.
Fellow, Montreal Neurological Institute with
W. Penfield from 1937–1939. Lecturer at
Queen’s University, Ontario from 1939 to
1941; Assistant Professor from 1941 to
1942. Involved in founding the Bulletin of
the Canadian Psychological Association
from 1940 to 1942.
Becomes President of the
Canadian Psychological
Association (CPA) in 1952.
Becomes President of
Division 3 of the American
Psychological Association
(APA) in 1953.
Research Associate with Lashley at
the Yerkes Laboratories of Primate
Biology from 1942 to 1947. Officially
employed as a Harvard University
Research Fellow from 1945 to 1947.
Professor of Psychology at McGill
University from 1947 to 1970, and
Chairman of the Psychology
Department from 1948 to 1958.
Becomes President of the
APA. Receives distinguished
scientific contribution award
from the APA in 1961, and an
award from the Association for
Research in Nervous Mental
Disorders in 1962.
Chancellor of
McGill University
from 1970 to
1974. Awarded
gold medal from
the APA in 1974.
Vice Dean of biological
sciences at McGill from 1964
to 1966. Nominated for the
Nobel Prize in 1965 and
awarded the Claude Bernard
Medal from the University of
Montreal in 1966.
Becomes Chairman of the
National Research Council
(NRC) Experimental
Psychology Committee.
Awarded the Warren Medal by
the Society of Experimental
Psychologists in 1958.
Timeline | Life and work of Donald O. Hebb
1904 1921 1928 1934 1937 1942 1952 1956 1960 1964 1970
Box 1 | Development of the ‘Hebb synapse’ postulate: 1932
The Organization of Behavior is still cited frequently, mostly referring to Hebb’s
neurophysiological postulate:“when an axon of cell A is near enough to excite a cell B and
repeatedly and persistently takes part in firing it, some growth process or metabolic change takes
place in one or both cells such that A’s efficiency, as one of the cells firing B,is increased.”Neural
network designers adopted this learning postulate,referring to it as the Hebb rule, and some
years later neurophysiologists devised techniques for testing the postulate
55,56
.Synapses that
conformed to the rule were eventually called ‘Hebb synapses’
57
.
Hebb’s idea first appears in his M.A.thesis, Conditioned and Unconditioned Reflexes and
Inhibition
12
.To follow his train of thought,it is useful to understand the climate in psychology at
the time. The English translation of Pavlov’s book Conditioned Reflexes was published in 1927
and created quite a stir.In 1928, Ariëns Kappers published his theory of neurobiotaxis
58
,
proposing that axons, regardless of whether they are being fired,grow towards active cells during
development.In 1925, Sherrington had published a paper on reflex inhibition
59
.
Hebb’s M.A.thesis shows the influence of
these publications. In this figure,he shows
that axons fired by a stimulus during the
elicitation of a reflex are attracted to the
active effector and become able to fire it.
Fired axons passing close to neurons that are
not active during the reflex retreat from
those neurons.Hebb’s summary of this
proposal in his thesis is:“An excited neuron
tends to decrease its discharge to inactive
neurons,and increase this discharge to any
active neuron,and therefore to form a route
to it, whether there are intervening neurons
between the two or not.With repetition this
tendency is prepotent in the formation of
neural routes.”
12
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PERSPECTIVES
association model, on which behavioural
learning theory was based at that time. He
attributed its adoption to an overzealous
attempt to avoid the ‘little man in the head’
fallacy.Hebb’s theory lays great emphasis on
stimulus–stimulus (S–S) association.
A second important problem involved
perception.It is clear that visual recognition
does not depend on the excitation of a specific
group of receptors.Circles of different sizes
and retinal position are all readily recognized
as circles,although they cannot be stimulating
the same receptors. Similar generalization
takes place in other modalities.This is difficult
to reconcile with the evidence that the traces
that are responsible for recognition are struc-
tural, involving, for example, changes in
synaptic strength of specific neurons. Separate
neural structures for the recognition of every
object at every size and position would
require more neurons than we possess.
Regarding the first problem,Hebb points
out that neo-Pavlovian learning theory,
although officially non-physiological,was in
fact based entirely on an out-of-date anatomi-
cal map,in which receptor organs,such as
the eye and the ear,feed input to the brain,
and paths leading from the brain deliver
its output to muscles and other effectors.
the functions of the frontal lobes
21,22
.Hebb
showed that removal of large portions of the
frontal cortex had little effect on intelligence,
as measured by the standardized tests of the
time.Hebb was most impressed by the patient
K.M.
21
,whose frontal lobes had been oper-
ated on by Penfield to remove epileptic foci.
Hebb noted that removal of tissue constituting
one third or more of each frontal lobe resulted
in “a striking post-operative improvement in
personality and intellectual capacity”
21
,Hebb’s
theory that the frontal lobes are important
only for learning during early life had an
important influence on the view of the brain
that he presented in The Organization of
Behavior.
Hebb never studied patients again after he
left the MNI in 1939,but after he returned to
McGill in 1947, he collaborated with Penfield
through his students and colleagues.These
included Mortimer Mishkin and H.Enger
Rosvold, who followed up his ideas on
the frontal lobes
23
,and Brenda Milner, who
extended Hebb’s ideas and techniques to
further explore the effects of temporal lobe
lesions
24
,most famously with patient H.M.
25
.
Developmental psychobiology
Inspired by his theory of the changing role of
the frontal lobes with age,Hebb began work-
ing on the development of rat intelligence.At
Queen’s University, where he was appointed
to a teaching position in 1939,Hebb and a
student,Kenneth Williams, designed a vari-
able path maze
26
.The Hebb–Williams maze
has since been used in a plethora of studies of
comparative learning in animals
27
.
To determine the effects of early experience
on learning, Hebb used this and other mazes
to test rats blinded at different ages,and rats
reared as pets at home versus rats reared in
laboratory cages. He showed that enriched
experience during development resulted in
improved maze learning in adulthood
28
,and
he concluded “there is a lasting effect of infant
experience on the problem-solving ability of
the adult rat.”These ideas formed the basis
of one of the most powerful concepts in devel-
opmental psychology,leading to the establish-
ment of ‘early start’programmes to enrich the
experiences of underprivileged children in
reading, writing and mathematical abilities,
and in music,sports and art (Head Start)
29
,
and studies on the effects of environmental
stimulation on neural development
30
.They
still influence research today.He also showed
that the effects of brain damage on the devel-
opment of intelligence depended on the age
when the damage occurred
31
.
The Organization of Behavior
In 1942, Lashley moved to Orange Park,
Florida, to replace Yerkes as Director of the
Ye rkes Laboratories of Primate Biology, and he
invited Hebb to join his team to investigate
chimpanzee behaviour. Hebb’s role was to
develop tests of emotion that could be used
with normal and brain-lesioned animals.
Lashley was to investigate learning, but he
found chimpanzees more difficult to teach
than rats, and no chimpanzees were operated
on during the five years of Hebb’s fellowship.
Hebb did, however, develop several tests
for fear and anger expression in intact
chimpanzees
32
.
The research proceeded slowly, but the
intellectual climate was stimulating.By the end
of his five-year fellowship, in addition to
several papers on emotionality
32,33
and dolphin
behaviour
34
,Hebb had completed the manu-
script of a book,eventually published under
the title The Organization of Behavior. In
this book,he outlined an entirely new way of
relating brain and behaviour, based on the
conviction, not then prevalent among psychol-
ogists, that the only scientific way to explain
behaviour was in terms of brain function.
Hebb summarized with great clarity some
of the problems confronting psychologists in
the middle of the twentieth century, and
outlined his solutions for them.The first prob-
lem concerned ‘mental’ processes, such as
attention and determining tendency, that
were generally acknowledged to be important,
but that had been declared off-limits for
psychologists by the dominant school of
neo-Pavlovian behaviourists. Hebb was critical
of the Pavlovian stimulus–response (S–R)
NATURE REVIEWS | NEUROSCIENCE VOLUME 4 | DECEMBER 2003 | 1015
Hebb dies on
20 August.
1977 1985 2003
Figure 1 | Chester, Nova Scotia. Donald O. Hebb
at his summer home in 1942, with daughters Jane
at his side and Mary Ellen on his shoulder. Photo
courtesy of Mary Ellen Hebb.
Inducted into the
Canadian Medical
Hall of Fame in
October 2003.
Appointed Honorary Research
Associate at Dalhousie University.
Becomes Professor Emeritus in 1978.
Receives Society for Research in
Child Development Distinguished
Scientific Contribution Award in 1979
and CPA Distinguished Scientific
Contribution Award in 1980.
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PERSPECTIVES
Even some of the psychological data that
was available to Hebb proved to be unreliable.
Lashley was convinced,on the basis of his 1929
rat maze experiments, that the non-sensory
cortex is equipotential for learning
37
.Present-
day imaging methods show this to be far from
the case.Hebb also believed that perceptual
learning developed slowly, whereas we now
know that infants can recognize some objects
by sight within a few hours of birth,and might
learn about some sounds even before birth.
Nevertheless, Hebb employed this
unpromising material with great ingenuity to
conjure up cell-assemblies and chains of cell-
assemblies, linked by the neural activity
accompanying eye movements that he called
phase-sequences. Hebb envisioned phase-
sequences as neural representations of images
and concepts.Many psychologists were dis-
illusioned by the rarefied philosophy of the
neo-Pavlovians, so these constructs were
received with great enthusiasm.The Hebb of
1945 would not have recognized the nervous
system of 2003, but if it had been accessible to
him when he was writing his book, who
knows what a wonderful psychological theory
he would have woven from it?
Hebb acknowledged that his theory would
need revision in the light of new discoveries.
All theories are built on the shifting sand of
experimental data, and the sand on which
Hebb built shifted unusually quickly, partly as
school of thought for the explanation of gener-
alization was that sensory input establishes a
field,perhaps electrical, in the brain.The form
taken by the field was stipulated to depend only
on the pattern of the stimulus, and not on the
specific location ofthe stimulated receptors,so
similar patterns always gave rise to the same
field. Gestalt theory could not explain how
recognition of the field was acquired,however.
When this question arose, the Gestalt answer
was that recognition took place in the mind.
The rival behaviourist school of thought,
on the other hand,could explain the learning
but was vague as to how a pattern falling on
different receptors could reach the same
learned recognition structure.Hull
36
suggested
that it was by “afferent neural interaction”, but
did not explain how that process might work.
Hebb thought that these problems could
be solved by the application of up-to-date
neural data, and he claimed that his theory
did just that. Unfortunately, however, the
anatomy and physiology of the 1940s was
only marginally better than that of the 1920s.
Little was known about the structure and
connections of the neocortex,and even less
was known about the anatomical connections
between and within subcortical and brain-
stem nuclei.Synaptic transmission was still
believed to be electrical,making inhibition,
the action of psychoactive drugs, learning,
neural effects lasting for longer than a few
milliseconds and many other neural mecha-
nisms much more difficult to understand
than they are today,now that we know that
most synaptic transmission is chemical.
Classical learning theory attempted to formu-
late what happens to the information during
this journey. Because neurons conduct in only
one direction, the route was misguidedly
assumed to be ‘one way’. Furthermore, the
entire transmission path was postulated to be
passive,adding nothing to the input signal.
This made it difficult,if not impossible, for the
theory to take account of mental processes like
intention or desire,should such ‘heresy’ever
be contemplated.
Hans Berger’s announcement, in 1929
(REF 35), that the brain exhibits continuous
electrical activity changed all this.Simple equa-
tions could no longer be considered as realistic
representations of the S–R relationship in
living organisms; the intrinsic activity of the
path must be taken into account.For Hebb,
this meant that psychologists could no longer
pretend that the biology of the organism is
irrelevant. If, as seems obvious, behaviour
is affected by variables like attention and set,
psychological theory cannot ignore them.The
phenomena must be related to neural activity,
and if current neural data cannot explain
them,the only scientifically acceptable conclu-
sion is that current data are wrong or incom-
plete.Hebb pointed out that electroencephalic
data clearly demonstrated the inadequacy of
the physiological data on which classical
behaviourism rested.This was Hebb’s justifica-
tion for adopting a neural theory based on
more current neurophysiological data.
Generalization in the visual system was the
main issue that was tackled by Hebb in The
Organization of Behavior
(BOX 3)
.The Gestalt
Box 2 | Development of the ‘Hebb synapse’ postulate: 1934
As a Ph.D. student at the University of Chicago in 1934, Hebb re-applied his ideas in a paper for
his anatomy class,entitled ‘The interpretation of experimental data on neural action’. One of the
figures from this paper (panel a) illustrates the Hebb synapse principle.A represents an afferent
axon excited by the stimulus to be conditioned,and X and Y represent efferent tracts leading to
the active reflex and to other less active reflexes.The co-incidence of excitation in A and reflex
activity in X would lead to the formation of a route A–B–X and to the discontinuance of other
routes, such as A–C–Y,A–D and A–E. So,to explain the acquisition of conditioned reflexes,
Hebb modified the neurobiotaxis theory in two ways: 1) only active axons would grow towards
active target cells,and 2) active axons would be repelled by inactive cells.Another figure from
this paper (panel b) expands this concept to an axon A with two terminal branches A’and A’’
activating B and C.With greater activity of B, the route A’–B will be strengthened,but if there is
an interneuron D, which is activated by A’,the route A’–D–C will be strengthened.
Figure 2 | Dalhousie University. Donald O. Hebb
at Dalhousie University, circa 1922. Photo
courtesy of Mary Ellen Hebb.
a
b
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PERSPECTIVES
and Sharpless on sensory deprivation was
reported in the Montreal Gazette of 14
January 1954 under the headline “See, hear,
feel nothing research shows bored brain acts
queerly: isolation tests at McGill pay human
guinea pigs $20 a day — but few can take it.”
The same research was treated more harshly in
the New York Times of 15 April 1956,which
linked Hebb’s sensory deprivation experi-
ments at McGill to brainwashing. The
Montreal Gazette of 26 April 1956 ran a front
page headline “Brainwashing defense found”
and a second article entitled “McGill discovery
will benefit military”, which explained how
the Defense Research Board of Canada
had contracted the experiments on sensory
deprivation to study “so-called brainwashing ...
used by opponents of western powers.”This
was at the time ofthe Korean War (1950–1953),
and the introduction of the term ‘brainwash-
ing’in Edward Hunter’s book Brainwashing
in Red China (1951) led to the fear of commu-
nist brainwashing of captured soldiers.
a consequence of his own activities.The fact
that a large part of his structure remains
intact today is a tribute to his intuition.He
knew better than the physiologists what sort
of brain would be needed to produce the
behaviour he observed. Though the material
he used was primitive and faulty,he lashed
it together into something that served his
purpose, which was primarily to promote the
idea that the future of psychological theory
lay in the arms of the neural sciences.In this,
he succeeded far beyond his expectations.
In 1949 Hebb stood at the crossroad,
pointing out the new road called neuro-
science,which psychologists and biologists
with an interest in the nervous system and
behaviour could take together to reach their
common goals. The enduring value of Hebb’s
writing stems from this vision. Few people
today would defend the nuts and bolts of
Hebb’s neuropsychological theory of percep-
tual learning, but it provided a goal towards
which psychological theory should move,and
showed what could be done as anatomical
and physiological knowledge expanded.The
ensuing progress in that direction more than
justifies the acclaim that Hebb’s speculations
have enjoyed for the last half-century.
Hebb as teacher and administrator
During the 1950s and his later years (FIG.3),
Hebb’s name was associated less with research
papers and more with theoretical reviews and
administrative and educational issues. At
McGill, Hebb taught introductory psychology
classes, wrote a textbook of psychology
38
(which was reprinted four times),and taught
a graduate research seminar. Hebb developed
an idiosyncratic philosophy of graduate edu-
cation
39
,in which he stated that you cannot
train students to do research,but you can set
up the conditions for them to do research. For
example, you can encourage them to start
research projects early in their career; prevent
them from taking too much coursework or
formal examinations; help them in choosing a
research problem and in making a success of
their project, and train them to write. He
believed that students should be evaluated on
their intelligence and motivation to do
research,and their ability to think and do,
rather than to memorize the work of others.
Hebb defined psychology as a biological
science
40
and stated that it should be studied
by objective methods, rather than by intro-
spective,humanistic or subjective methods
that are more suited to literature and the arts.
Like Lashley, Hebb saw the subject matter of
psychology as the mind and the capacity for
thought, and he defined thought biologically,
as the integrative activity of the brain. Hebb’s
focus on the biological bases of behaviour
and his methods for training students turned
McGill into the foremost centre for physio-
logical psychology (behavioural neuro-
science) in the world.The success of Hebb’s
educational methods are reflected in the suc-
cess of his students, including Bernard
Hymovitch, Donald Forgays, Mortimer
Mishkin,Brenda Milner, Peter Milner,Ronald
Melzack,Seth Sharpless,Woodburn Heron,
Helen Mahut, Gordon Mogenson, Case
Vanderwolf and legions of others who
attended his introductory psychology class
and graduate seminar and were motivated to
pursue biological psychology as a career.
During the 1950s, work from Hebb’s labo-
ratory was often front-page news in the
Montreal newspapers.For example,the work
of Olds and Milner was reported on the front
page of the Montreal Gazette on 12 March
1954,under the headline “McGill opens vast
new research field with brain ‘pleasure area’
discovery.”The work of Bexton, Heron, Scott
NATURE REVIEWS | NEUROSCIENCE VOLUME 4 | DECEMBER 2003 | 1017
Box 3 | Development of the ‘Hebb synapse’ postulate: 1949
In the late 1940s,Hebb was confronted with the problem of how a random collection of
neurons could be organized by visual stimuli to allow the subsequent recognition of the stimuli.
Once more he resorted to his learning postulate.Possibly because the neurobiotaxis idea was
strongly criticized during the intervening years,the 1949 postulate differs in two respects from
that of his thesis. First,Hebb introduced metabolic change as a possible alternative to growth as
a means of changing the effectiveness of a connection. Second,there is no mention of the
withdrawal of axons from inactive neurons.This second aspect of the theory has been criticized
because it only predicts increases in synaptic strength.Ironically, recent research
43
shows that if
neuron A of Hebb’s postulate,instead of contributing to the firing of neuron B,fires after B has
already fired,the connection between A and B is weakened,as Hebb originally proposed. The
figure illustrates Hebb’s hypothetical cortical circuit to explain how his learning postulate was
involved in the growth of cell assemblies
1
.
In 1973,Bliss and Lomo
60
reported long-term potentiation (LTP) of synaptic transmission in
hippocampal neurons after tetanic stimulation of an afferent path. This could have been the
result of a diminished synaptic resistance,but in 1994 Lin and Glanzman
61
showed that if a cell
was hyperpolarized to prevent it from firing during stimulation of the afferent path,it showed
no LTP. So, nearly a decade after his death,it was confirmed that at least some neurons behaved
in accordance with Hebb’s neurophysiological postulate. Figure reproduced,with permission,
from The Organization of Behavior Mary Ellen Hebb.
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PERSPECTIVES
substantially.Interestingly,the fiftieth anni-
versary of The Organization of Behavior
stimulated more reviews
2,44,47–49
than appeared
in the years just after the original publication
49
.
Hebb’s ideas are the basis of special issues of the
Canadian Journal of Experimental Psychology
(March 1999) and Biological Cybernetics
(December 2002). Four papers on the
Hebb rule and Hebb synapse appeared in
the February 2003 issue of Canadian
Psychology
50–53
.But the greatest tribute to Hebb
was probably paid by Adams
54
,who stated that
“Two of the most influential books in the
history of biology are Darwin’s On the Origin
of Species (1859/1964) and Hebb’s The
Organization of Behavior (1949).”
Richard E.Brown is at the Department of
Psychology, Dalhousie University, Halifax,
Nova Scotia B3H 4J1, Canada.
Peter M. Milner is at the Psychology Department,
McGill University, 1205 Avenue Dr. Penfield,
Montreal PQ H3A 1B1,Canada.
Correspondence to R.E.B.
e-mail: rebrown@dal.ca
doi:10.1038/nrn1257
1. Hebb, D. O. The Organization of Behavior; a
Neuropsychological Theory (Wiley, New York, 1949)
(reprinted by Lawrence Erlbaum Associates, 2002).
2. Seung, H. S. Half a century of Hebb. Nature Neurosci. 3,
Suppl. 1166 (2000).
3. Fentress, J. C. The Organization of Behavior revisited.
Can. J. Exp. Psychol. 53, 8–20 (1999).
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psychobiology: 1904–1985. Behav. Brain Sci. 8, 529
(1985).
5. Fentress, J. C. D. O. Hebb and the developmental
organization of behavior. Dev. Psychobiol. 20, 103–109
(1987).
6. Klein, R. M. The Hebb legacy. Can. J. Exp. Psychol. 53,
1–3 (1999).
7. Milner, P. M. The mind and Donald O. Hebb. Sci. Am.
268, 124–129 (1993).
8. Hebb, D. O. D. O. Hebb. in A History of Psychology in
Autobiography Vol. VII (ed. G. Lindzey) 273–309 (W. H.
Freeman, San Francisco, 1980).
9. Hebb, D. O. Elementary school methods. Teacher’s
magazine 12, 23–26 (1930).
10. Sherrington, C. The Integrative Action of the Nervous
System (Yale Univ. Press, New Haven, 1906).
11. Pavlov, I. P. Conditioned Reflexes (Dover Publications,
New York, 1927).
12. Hebb, D. O. Conditioned and Unconditioned Reflexes
and Inhibition. M.A. Thesis, McGill Univ. (1932).
13. Hebb, D. O. Essay on Mind (Erlbaum, Hillsdale, New
Jersey,1980).
14. Dewsbury, D. A. The Chicago five: a family group of
integrative psychobiologists. Hist. Psychol. 5, 16–37 (2002).
15. Hebb, D. O. The innate organization of visual activity:
I. Perception of figures by rats reared in total darkness.
J. Gen. Psychol. 51, 101–126 (1937).
16. Hebb, D. O. Studies of the organization of behavior.
I. Behavior of the rat in a field orientation. J. Comp.
Psychol. 25, 333–353 (1938).
17. Hebb, D. O. Intelligence in man after large removals of
cerebral tissue: report of four left frontal lobe cases.
J. Gen. Psychol. 21, 73–87 (1939).
18. Hebb, D. O. & Morton, N. W. Note on the measurement
of adult intelligence. J. Gen. Psychol. 30, 217–223
(1944).
19. Hebb, D. O. Intelligence in man after large removals of
cerebral tissue: defects following right temporal
lobotomy. J. Gen. Psychol. 21, 437–446 (1939).
20. Hebb, D. O. & Morton, N. W. The McGill adult
comprehension examination: verbal situation and picture
anomaly series. J. Educ. Psychol. 34, 16–25 (1943).
21. Hebb, D. O. & Penfield, W. Human behavior after
extensive bilateral removal from the frontal lobes. Arch.
Neurol. Psychiatry 42, 421–438 (1940).
honorary doctorates by 15 universities and was
nominated for the Nobel Prize in Physiology
and Medicine in 1965.
Hebb’s legacy
The legacy of Hebb is found in every area of
psychology and neuroscience.Modern neuro-
psychology is based on Hebb’s work with
Penfield,the study of environmental effects
on development derives from Hebb’s pet rats
reared at home in an enriched environment,
and computer models of the brain are based
on Hebb’s ideas of the synapse and cell assem-
bly.Also,the physiological bases of learning
and memory are based on Hebb’s ideas of
multiple memory systems, and long-term
potentiation (LTP) is the experimental analy-
sis of Hebbian synaptic plasticity. Hebb’s
frequent emphasis on the effects of the timing
of neural impulses on brain function is
in keeping with the recent discovery of
spike-time-dependent synaptic plasticity
44,45
,
and the work of Hubel and Wiesel on neural
plasticity of sensory system development was
inspired by the first five chapters of The
Organization of Behavior.In addition,studies
of the neural bases of emotion, motivation,
reward and pain derive from Hebb’s ideas and
the research of his students.
Hebb’s ideas have stood the test of time
and have become the central tenets of psycho-
logy and neuroscience. Although a 2002
study
46
ranked Hebb as only the nineteenth
most eminent psychologist of the twentieth
century, a greater awareness of what we
owe to Hebb should increase this ranking
Although aspects of Hebb’s sensory depriva-
tion experiments are still classified as secret,
most of the results have been published,
including a summary in Scientific American
41
.
Hebb’s belief that the biological basis of the
mind is the proper study of psychology, com-
bined with his conceptual focus on the
synapse and the cell assembly, allowed him to
apply his ideas on the biological basis of
behaviour to social and clinical psychology,
motivation,perception,thought and the study
of consciousness. In his presidential address to
the Experimental Division of the American
Psychological Association
42
,Hebb incorpo-
rated the newly discovered reticular arousal
system into his theory to explain optimum
levels of arousal for different tasks,and in the
Handbook of Social Psychology,Hebb and
Thompson
43
examined the social importance
of animal research for human behaviour as an
approach to the biological basis of behaviour.
Hebb’s 1980 book Essay on Mind
13
is a
summary of his ideas on the biological basis of
mind.It is also a sequel to The Organization of
Behavior and a completion of the unfinished
book he started to write in 1933, in which the
first chapter was entitled ‘The conception of
mind’ bringing his writing full circle from
1980 back to 1933.
Hebb was the chairman of the Psychology
Department at McGill from 1948 to 1958 and
Vice Dean of biological sciences from 1964 to
1966. After his ‘retirement’, he was elected
Chancellor of McGill University from 1970 to
1974.Throughout his career, Hebb received
many honours
(TIMELINE).He was given
Figure 3 | Montreal Neurological Institute. Donald O. Hebb delivering the Hughlings Jackson Lecture in
1958. Photo courtesy of Mary Ellen Hebb.
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PERSPECTIVES
56. Kupfermann, I. & Pinsker, H. in Biology of Memory (eds K.
H. Pribram & D. E. Broadbent) 163–174 (Academic
Press, New York, 1970).
57. Rauschecker, J. P. & Singer, W. The effects of early
experience on the cat’s visual cortex and their possible
explanation by Hebb synapses. J. Physiol. (Lond.) 310,
215–239 (1981).
58. Kappers, A. Three Lectures on Neurobiotaxis
(Heinemann, London, 1928).
59. Sherrington, C. S. Remarks on some aspects of reflex
inhibition. Proc. R. Soc. Lond. B 97, 519–545
(1925).
60. Bliss, T. V. & Lomo, T. Plasticity in a monosynaptic cortical
pathway. J. Physiol. (Lond.) 207, 61P (1973).
61. Lin, X. Y. & Glanzman, D. L. Hebbian induction of long-
term potentiation of Aplysia sensorimotor synapses:
partial requirement for activation of an NMDA-related
receptor. Proc. R. Soc. Lond. B 255, 113–118
(1994).
Acknowledgements
We would like to thank the McGill University archives for access to
Hebb’s files, and Mary Ellen Hebb and Jane Hebb Paul for access
to family photographs and letters.
Competing interests statement
The authors declare that they have no competing financial
interests.
Online links
FURTHER INFORMATION
American Psychological Association: http://www.apa.org/
Canadian Psychological Association: http://www.cpa.ca/
Head Start Bureau:
http://www2.acf.dhhs.gov/programs/hsb/
International Society for the History of Neuroscience:
http://www.bri.ucla.edu/nha/ishn/
Montreal Neurological Institute: http://www.mni.mcgill.ca/
National Head Start Association: http://www.nhsa.org/
Yerkes National Primate Research Center:
http://www.emory.edu/YERKES/
Access to this interactive links box is free online.
22. Hebb, D. O. Man’s frontal lobes: a critical review. Arch.
Neurol. Psychiatry 54, 10–24 (1945).
23. Rosvold, H. E. & Mishkin, M. Evaluation of the effects of
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122–126 (1950).
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Psychol. Bull. 51, 42–62 (1954).
25. Scoville, W. B. & Milner, B. Loss of recent memory after
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Psychiatry 220, 11–21 (1957).
26. Hebb, D. O. & Williams, K. A method of rating animal
intelligence. J. Gen. Psychol. 34, 59–65 (1946).
27. Brown, R. E. and Stanford, L. The Hebb–Williams Maze:
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23, 110.14 (1997).
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solving at maturity. Am. Psychol. 2, 306–307 (1947).
29. Mann, E. T., Elliot, C. C. Assessment of the utility of
project Head Start for the culturally deprived: an
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unilateral and bilateral eye closure on cortical unit
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test scores, and the nature of normal adult intelligence.
Proc. Am. Phil. Soc. 85, 275–292 (1942).
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34. McBride, A. F. & Hebb, D. O. Behavior of the captive
bottle-nose dolphin, Tursiops truncatus. J. Comp.
Physiol. Psychol. 41, 111–123 (1948).
35. Berger, H. Über das Elektrenkephalogramm des
Menchen. Archiv Für Psychiatrie und Nervenkrankheiten
(Berlin) 87, 527–570 (1929).
36. Hull, C. L. Principles of Behavior: An Introduction to
Behavior Theory (Appleton-Century, New York, 1943).
37. Lashley, K. S. Brain Mechanisms and Intelligence: a
Quantitative Study of Injuries to the Brain (Univ. Chicago
Press, Chicago, 1929).
38. Hebb, D. O. A Textbook of Psychology (Saunders,
Philadelphia, 1958).
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(1973).
NATURE REVIEWS | NEUROSCIENCE VOLUME 4 | DECEMBER 2003 | 1019
CORRECTION
THE HIGH-CONDUCTANCE STATE OF NEOCORTICAL
NEURONS IN VIVO
Alain Destexhe, Michael Rudolph and Denis Paré
Nature Rev. Neurosci. 4, 739–751 (2003)
In Figure 6b, the abscissa should read “Input frequency (Hz)”. The legend to figure 6b should read “The right panels show
examples of interspike interval (ISI) histograms for stimulation at 4 ms and 12 ms interstimulus intervals, for the quiescent
(bottom) and high-conductance (top) states.”
CORRECTION
MYELIN-ASSOCIATED INHIBITORS OF AXONAL REGENERATION
IN THE ADULT MAMMALIAN CNS
Marie T. Filbin
Nature. Rev. Neuroscience 4, 703–713 (2003)
In box 2,the second sentence of the second paragraph should read “how can this be the case when sialic acid-dependent
binding seems to be non-essential for Mag to bring about inhibition?”
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