And Pavlov still rings a bell - Springer Static Content Server

J Neurol
DOI 10.1007/s00415-015-7858-5
ELECTRONIC SUPPLEMENTARY MATERIAL
And Pavlov still rings a bell: summarising the evidence for the use
of a bell in Pavlov’s iconic experiments on classical conditioning
S. Jarius1 • B. Wildemann1
Received: 2 July 2015 / Revised: 9 July 2015 / Accepted: 12 July 2015
Abstract The iconic ‘dog-and-bell scenario’ used to illustrate the concept of classic conditioning developed by the
Russian physiologist Ivan Petrovich Pavlov (1849–1936)
in most textbooks in the field of neurophysiology and psychology has been repeatedly put into question. Here, we
summarise and critically discuss the available evidence for
and against the occasional use of a bell in Pavlov’s laboratory from his own writings and those of his co-workers
and, in addition, re-present new pictorial evidence. We
conclude that the ‘dog-and-bell scenario’ indeed has a factual basis, but is strongly influenced by a verifiably incorrect 1928 report in the then widely read Time magazine.
Keywords Ivan Petrovich Pavlov; classical conditioning;
unconditioned stimulus; bell.
The term ‘classical conditioning’ (CC) is used to refer to a
process of learning that is induced by the repeated pairing
of a neutral stimulus (NS) with a potent biological stimulus
(so-called unconditional stimulus), eliciting a usually innate reaction (the so-called unconditional response, UR).
CC results in the NS becoming a more or less potent, socalled conditional stimulus able to elicit the UR (which
then is called a conditional response, CR). Although the
concept as developed by Pavlov has been repeatedly challenged, it has become the foundation of the modern science
 S. Jarius,
[email protected]
1
Molecular Neuroimmunology Group, Department of
Neurology, University of Heidelberg, Otto Meyerhof Center,
Im Neuenheimer Feld 350, 69120 Heidelberg, Germany
of learning and, in particular, of the influential theories of
Watson and Skinner and the entire school of behaviourism.
In a recent article on the life and achievements of the
Russian physiologist Ivan Petrovich Pavlov (1849–1936)
in the January 2015 issue of this journal [8], the authors
questioned whether Pavlov ever used a bell in his experiments on CC: “Nowadays, we reflexively link his name to a
dinging bell and a drooling dog, although he never trained
a dog to salivate to the sound of a bell [8]. Our brains
have been conditioned with [a] myth” [8]. This is in line
with at least three previous authors who stated they
“hunted in vain for any such mention” [7] or “have not yet
found any experiment in which a bell was used” in Pavlov’s works [9, 16].
However, this notion has been refuted by others and
characterised as “the myth of a myth” [26].
To shed some more light on this issue we decided to
investigate the evidence in favour of Pavlov’s use of a bell
in more detail. Given that the ‘dog-and-bell scenario’ is
described in almost all major textbooks and has become
‘common knowledge’, this seems to be a matter of more
general interest.
To clarify the issue further, we first screened all of
Pavlov’s works included in the two volumes of the 1941
edition of Lectures on Conditioned Reflexes (Volume 1:
Twenty-five years of objective study of the higher nervous
activity (behaviour) of animals; volume 2: Conditioned
reflexes and psychiatry) [21], which contains a compilation
of Pavlov’s speeches and articles. Both volumes were
translated and edited by W. Horsley Gantt, a pioneer in
psychophysiology, whose work is reflected in seven books
and more than 700 publications [14]. Gantt was a coworker of Pavlov from 1925 to 1929 and later director of
the Pavlovian Laboratory at Johns Hopkins University as
well as initiator and long-standing editor of the Conditional
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DOI 10.1007/s00415-015-7858-5
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Reflex Journal (published under the auspices of the Pavlovian Society); he can thus be considered a credible
source. Of note, his 1941 edition also contains Pavlov’s
later writings, published between 1928 and his death in
1936.
By contrast, previous authors interested in the “dogand-bell” riddle [7, 9, 16, 26] mainly used Gleb Vassilievitch von Anrep’s (1891-1955) [10] 1927 edition of
Conditioned reflexes. An investigation of the physiological
activity of the cerebral cortex [17] – a different book from
that translated by Gantt despite the similar title.
In Gantt’s edition of Pavlov’s works, we found numerous mentions of a “bell”. In Destruction of the skin
analyser (read before the Society of Russian Physicians
and published in Transactions of the Society of Russian
Physicians, 1910–1911) Pavlov reports a series of experiments based on observations by N. M. Saturnov from his
laboratory. He gives a very clear description of the typical
CC experiment to which most modern textbooks refer:
“You see that the dog is now quiet, and that saliva
does not flow spontaneously. The bell begins to ring. The
dog moves and looks for food, and 9 drops of saliva appear
– clearly a normal reaction. The bell is obviously a conditioned stimulus. This demonstration is so evident that it is
not necessary to show you other sound reflexes.” (vol. I, p.
166)
A bell is also mentioned in Scientific study of the socalled psychical processes in the higher animals (vol. I, p.
89), in Internal inhibition and sleep – one and the same
process (vol. I, p. 312), and in The inhibitory type of nervous systems in the dog (vol. I, p. 364-365, “the former
strongest of all the conditioned stimuli, viz., the bell”),
where we read:
“All the auditory reflexes were one and a half times or
twice as great as the optical. The bell occupied first place
among the sounds, next came the metronome, and the
weakest of all was the whistle.” (p. 364).
In A physiological study of the types of nervous systems, i.e., of temperaments (p. 372), Pavlov states:
“If you whistle, or ring a bell, or raise the hand, or
scratch the dog – whatever you will – and now give the dog
food and repeat this several times, then each one of these
stimuli will evoke the same food reaction: the animal will
strive toward the stimulus, lick his lips, secrete saliva, etc.,
– there will be the same reflex as before”.
Of note, Pavlov still mentioned a bell (besides a rattle)
in some of his latest works (cf. vol. II, chapters XLVII and
LVII of the 1941 edition of Gantt’s English translation).
A bell is also explicitly mentioned in Gantt’s introduction to his translation of Pavlov’s Lectures: “The intensity
of the conditioned reflex has been shown (…) by Pavlov
(…) to depend also upon the intensity of the conditioned
stimulus – a loud bell produces a greater food excitation
than a faint one (…) within certain ranges” (p. 13 of the
1941 edition). Here, Gantt possibly referred to a work by
Kupalov, Lyman and Lukov from Pavlov’s laboratory published in 1931 in Brain [15] that indeed made use of a bell.
Finally, Pavlov’s refers to a bell also in his famous
Huxley lecture read at Charing Cross in 1906, which was
published in The Lancet [19] (and, and in a condensed
form, in the British Medical Journal [20]). However, the
lecture was “[s]pecially translated for The Lancet” and the
original version is, to the best of our knowledge, lost†.
While the wording of Gantt’s version of that lecture is different from that published in The Lancet [19], both translations consistently use the phrase “ringing of a bell” when
speaking about acoustic stimuli.
However, it is not completely clear what types of bells
were used. In his 1927 translation of the third lecture in
Pavlov’s Conditioned reflexes: an investigation of the
physiological activity of the cerebral cortex (1927; Dover,
New York), in which an experiment illustrating the development of a secondary conditioned reflex is described
(Lecture III), Anrep mentions an ‘electric bell’‡:
“A dog has two primary alimentary conditioned stimuli
firmly established, one to the sound of a metronome and
the other to the buzzing of an electric bell.” (p. 34)
Going back to the Russian original text [27], we found
that where Anrep writes, “the buzzing of an electric bell”,
Pavlov simply used the single word “звонок”. The same
word, in other instances, was translated as “bell” by Gantt.
By contrast, in Lecture VIII, in which Pavlov speaks
about compound stimuli, Anrep confusingly uses the word
“bell”, too, where Pavlov has “звонок”:
“In other experiments the stimulatory compound was
made up of three or four different stimuli all belonging to
one analyser; the stimuli were made to succeed one another in a definite order, being each of equal duration, and
with equal pauses between them. There were used, for example, in one case the four tones C, D, E, F of one octave;
and in another case the four stimuli were made up of a
noise, two different tones and the sound of a bell.”
Did Anrep have more detailed knowledge of the setup
of those experiments that allowed him to make such specific distinctions? It seems highly unlikely that specific
†
According to a report in Science [18] and as suggested by the many
German terms given in parenthesis in the English translation [19], the
speech was originally delivered by Pavlov in the German language.
‡
Electric bells were invented in the 1830s [13] and had become commonplace by the early 1900s.
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changes to the text such as those in lecture III were not
made deliberately: Like Gantt, he had been a close collaborator of Pavlov in the past and worked with auditory stimuli himself [5]§. Moreover, (in the foreword to his edition)
he emphasised that all changes he introduced to the original text were made with the agreement of Pavlov**.
However, it is also possible that this inconsistency reflects editorial negligence. First, Anrep, who was not a
native English speaker, employed (as he states in the same
foreword) professional translators funded by the Royal
Society to generate a draft translation of lectures I-XII,
which he then finalized. Second, he had to work under substantial time-pressure from the time he learned about
Gantt’s independent translation of Pavlov’s Twenty years
of objective study (appealing to Pavlov, Anrep could stipulate only a six months delay in publication of Gantt’s book
[25]).
On the other hand, Gantt was both a native English
speaker and had worked at Pavlov’s laboratory in Leningrad for altogether six years. Why would he not employ
the word buzzer, electric bell, or doorbell in his translations whenever such a device had been used?
In 1976, Gantt should still use the term “bell”. In that
interview (see [14] for a complete transcript), Gantt declares that he employed a “bell [as] the signal for food” in
his own laboratory at the Johns Hopkins University and
emphasises that he employed “the same methods” in his
dog experiments “as [he] had learned from Pavlov”.
Beside Gantt’s, there is a second personal testimony:
Tully (2003) refers to Petr Kuzmich Anokhin (1898–1974),
the father of the ‘feedback’ concept and one of the founders of the Institute of Psychology of the USSR and the
Laboratory of Neurophysiology of Training, as a witness.
According to Tully, Anokhin had “documented” the use of
“two bells” in Pavlov’s experiments, a “звонок” and a
“колоко́льчик" (the latter of those two words more transporting the idea of a traditional [hand]bell) [26].
In their abovementioned study, Kupalov and his colleagues concluded that “noises or more impure tones” (air
bubbling through water and, explicitly, a “bell” are given
as examples) produce stronger and more consistent conditioned reflexes than “pure (sine wave)” stimuli and specu-
lated that the auditory cortex of mammals may not be made
“for the hearing of tones but for the hearing of noises”,
suggesting that a non-electric bell may possibly have been
employed [15]. Kupalov’s findings, by the way, seem to
qualify, at least to some extent, the stance expressed in
Todes’ splendid recent book on Pavlov’s life, which has it
that the use of a bell would have been contra-intuitive since
Pavlov’s experiments required “precise control” of the
quality of the stimulus [25].
As the contemporary meaning of “звонок" (sometimes
we read “обычный [i.e. conventional] звонок” [15]) is not
unequivocal and as we could not find any account of the
word “колоко́льчик" in Pavlov’s writings, we set out to
look for pictorial evidence.
First, we screened a large number of original publications from Pavlov’s group for figures depicting the experimental setting. While this search was mostly unrevealing, we found an highly interesting image in Pavlov’s ‘official’ biography, published in 1953 by the Academy of
Science of the Soviet Union and authored by Pavlov’s pupil
Ezras Asratovich Asratyan (1903–1981), then head of the
Institute of Higher Nervous Activity and Neurophysiology
founded after the infamous ‘Pavlovian session’. This drawing of the dog chamber in Pavlov’s laboratory (Fig. 1) depicts a conventional bell (besides metronomes and a light
bulb, two other frequently employed stimuli) fixed to the
wall [6]. We are not aware of any previous publication on
the issue in question noting this image.
Second, we would like to draw attention to the 1926
Soviet educational film Mechanics of the Brain (original
Russian title Механика головного мозга), directed by
Vsevolod Illarionovich Pudovkin (1893-1953), an early
attempt to popularise Pavlov's studies in classical conditioning that was formerly accessible only at a few film institutes worldwide [24] but is now available as an internet
resource [23]. In contrast to other video footage [1], this
(silent) movie, filmed at Pavlov’s laboratory, indeed depicts the use of a conventional handbell (Fig. 2). To the
best of our knowledge, images from this sequence have
never been shown in print.
The film was made known to a Western medical audience for the first time in 1928 in New York [2] and, probably††, a second time in 1932 in Rome [22]. In 1960, an-
§
In this paper (reference [5]), Anrep mentions the use of a “simple
bell” as an extra stimulus able to inhibit the inhibition of a conditional
response.
**
“Professor Pavlov allowed me, for the sake of clarity, to introduce
some modifications and additions into the text in order to make the
reading lighter for those English and American readers unfamiliar
with the original literature in this field. This I have done sparingly,
being careful only to expand, but in no sense to alter, the original
meaning.” (p. viii) [17]
††
According to the opening captions of the 16 mm version, the film
was personally projected by Pavlov himself at the 14 th International
Physiological Congress [22]:
“This film was prepared by and under the direction of Ivan Petrovich Pavlov and was projected by him at the 16th International
Congress of Physiology in Rome in 1932. After the congress, Pavlov
donated the film to Carlo Foà who was then Professor and Chairman
of the Department of Physiology at the University of Milano Medical
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other English version (i.e. a 16-mm copy with English captions) was produced [22].
The movie was also made available to a broad lay audience. It was presented at cinemas from November 1928
(announced in the New York Times [12]) and was released
in the USA by Amkino Corp., as an educational film for
home projectors, at the latest in 1930 [3]. The latter was
described as “the famous Pavlov film” [3] and “a film digest [and] animated photographic record of the experiments and studies of a single individual, Professor Pavlov”
[12]. At the Fifth Avenue cinema, New York City, this
purely scientific movie, hardly an entertainment, was still
playing a month later, suggesting considerable interest on
the part of the public [11]; according to the Columbia
Daily Spectator, the playhouse was almost sold out [4].
Importantly, however, the short sequence showing the
use of a handbell does not depict the generation of a CR
but simply illustrates one of the “best known unconditioned [our emphasis] reflexes”, i.e. “the defensive reflexes” as the captions have it, going on to explain: “A
response to stimulation mediated through the subcortical
centers of the brain is called an unconditioned reflex”.
What is shown is simply “the response to a sudden
sound“. Only the subsequent sequence depicts the “study
of the alimentary unconditioned reflex”; there, a metronome rather than a bell is used as auditory stimulus.
In apparent contrast, the then widely read Time magazine reported in 1928:
“The process of changing an unconditioned reflex into
a conditioned reflex was clearly demonstrated to an audience of psychiatrists at the Academy of Medicine last week,
in a cinema entitled 'The Mechanics of the Brain.'
School. The film was used in Foà's course of medical physiology in
Milano and in Sao Paulo, Brazil, until his retirement. In 1960 the film
was brought to Detroit where 16 mm copies were made and the potentially explosive 35 mm original nitrate film was destroyed in compliance with fire safety regulations." – There is no doubt that Pavlov
attended the congress. Searching for independent confirmation regarding the presentation of that film, we found an entry in the catalogue of the British University Film & Video Council which lists a
film entitled ‘Functions of the Brain: Behaviour of Human and Animal’ (alternative title: ‘Functions of the Brain: Behaviour of Man and
Animal, Mechanism of the Brain’) and explains: “This silent film
features documentary footage of Ivan Petrovich Pavlov’s laboratory,
originally shown in 1932. It shows […] an experiment with children
who are fed cookies via a mechanical device to demonstrate conditioned responses; an experiment with a dog that demonstrates alimentary unconditioned reflexes; unconditioned reflex responses and
conditioned responses using food, sound or a shock plate. There is
also footage comparing child development from a newborn to a sixyear-old”. It seems that ‘Functions of the Brain’ (75 min) is an extended version of ‘Mechanics of the brain’ (1926 version: 35 min;
1928 version: 43 min).
The cinema showed dogs which dripped saliva at the
sound of a bell (...) if a bell is rung every time the food
appears, there will come a time when the dog will secrete
saliva at the sound of the bell when there is no food in
sight.
The simple reflex has been conditioned by the bell; the
dog has associated the food with the sound; the power
house of the upper brain has gone into action, and the intelligent animal now reacts to an idea.” [2]
Conceivably, therefore, a simple mistake by a Time
magazine reporter had a formative influence on the iconic
commonplace image of Pavlov’s experiments on CC involving a (conventional) bell. While the translation of
“звонок” as “bell” by Gantt, and previously by the translators of Pavlov’s 1906 Huxley lecture in The Lancet [19], as
pointed out by Todes [25] – may also have contributed to
this image, the Time magazine probably reached a broader
audience than both Gantt and The Lancet.
In summary, it seems from our research into Pavlov’s
publications and those of his co-workers that there is indeed sufficient evidence to corroborate the thesis that some
sort of bell was at least occasionally employed in CC experiments by Pavlov or his assistants. The statement that a
bell was never used [8] may thus be a little too harsh and
the ‘dog-and-bell scenario’ described in so many textbooks
may indeed have some factual basis. However, we found
only very limited evidence from a single drawing that the
bell used was indeed a conventional handbell. Moreover,
from our screening of Pavlov’s works it seems that other
stimuli may have been used more often than a bell. Finally,
we suggest that the iconic image of a dog being conditioned by use of a bell may well have been strongly influenced by a verifiably incorrect 1928 report in Time magazine.
Conflict of interest
The authors declare that they have no conflict
of interest.
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Fig. 1 Chamber for studying the conditional reflex (left, inner part; right, outer part) as depicted in Pavlov’s biography (1953/1974), authored by his pupil E. A. Asratyan, the later head of the Institute of
Higher Nervous Activity and Neurophysiology founded after the infamous ‘Pavlovian session’ (modified
image from [6]). Note the conventional bell (white arrow and inset) that is shown in addition to two metronomes and a light bulb (black arrows).
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Fig. 2 Scene from Pudovkin’s Mechanics of the Brain (1926), recorded at Pavlov’s laboratory in Leningrad. Note
the handbell used (arrowhead and inset). Of note, the scene shows an unconditioned response to an auditory stimulus. In another experiment depicted in the same film, a metronome is used as auditory conditioned stimulus.