Malmo 1963

ON CENTRAL AND AUTONOMIC NERVOUS SYSTEM
MECHANISMS IN CONDITIONING, LEARNING,

AND PERFORMANCE1
ROBERT B. MALMO2
Man Memorial Institute, McGill University
PSYCHOLOGY HAS COME A LONG WAY since physiological measures were

regarded simply as indices of emotion. One current line of research on
the autonomic nervous system (ANS) and behaviour is that of ANS
conditioning exemplified in the work of Black and his co-workers at
McMaster (Black, 1959; Black, 1961; Black & Carlson, 1957) and in the
experiments of Lacey and Smith (1954), and Notterman, Schoenfeld,
and Bersh (1952). I shall return to the subject of autonomic conditioning
experiments presently.
In our laboratory we have been concerned with the ANS in its corre-
lations with skeletal motor activity, electroencephalograms (EEGs),
incentive conditions, and performance. Initial experiments employed
skeletal muscle potential recording only (Bartoshuk, 1955a, 1955b) but
later experiments made use of various ANS measures in addition (Malmo
& Davis, 1956). Results from these and other experiments with human
subjects (Ss) which have been summarized elsewhere (Malmo, 1957)
encouraged the idea that physiological recordings made at the periphery
(i.e., from effectors) would tell us something about the nature of the
central nervous system (CNS) mechanisms mediating the observed
changes in performance. This work with human subjects preceded the
animal work to be described later and, in a very real sense, led up to it.
As I shall try to indicate in the following brief account, this rather long
1
This paper is an adaptation for publication of the presidential address delivered
at the Annual Meeting of the Canadian Psychological Association, Hamilton, Ontario,
June 1, 1962. Preparation of this review, and the research carried out in the author's
laboratory, were aided by a contract with the Surgeon General's Office of the U.S.
Army, and by grants from the National Institute of Mental Health (United States
Public Health Service), Department of National Health and Welfare (Canada),
National Research Council of Canada, and the Defence Research Board, Canada.
2
For critical reading of die manuscript I am indebted to J. S. Brown, D. O. Hebb,
G. A. Kimble, J. I. Lacey, P. F. MacNeilage, Celeste McCollough, Muriel H.
Stern, R. Elliott, Lucy Gardner, and ). M. Weiffenbach. I also wish to express my
gratitude to J. Olds for making his manuscript available to me in advance of publica-
tion. Drawings for Figures 2 and 6 were prepared by Helen MacArthur. The other
illustrations and charts were prepared by W. ] . Mundl whose invaluable assistance
in numerous ways is gratefully acknowledged, as is the painstaking work on the
manuscript by Constance Perkins.
1
CANAD. J. PSYCHOL., 1963,17(1)
2 ROBERT B. MALMO [Vol. 17, No. 1
series of related studies has yielded highly provocative findings. Though
sometimes it was necessary to work at a higher level of complexity than
one would like (e.g., with complicated incentive conditions) in psycho-
physiological experiments with human subjects there were, of course,
obvious advantages to be gained from including experiments with
human subjects in a neuropsychological research programme of this
kind. For one thing, the use of verbal instructions was invaluable as a
means of investigating important variables that are practically impos-
sible to investigate with animals. A good example is the phenomenon of
divided set that I shall discuss presently.
Bartoshuk's early work (1955a, 1955b) on muscle potentials in relation
to motivation and performance, and his later combined use of EEG and
electromyographic (EMG) recording in the study of startle (Bartoshuk,
1959) clearly influenced the course that our research has taken. Stennett's
(1957) experiment was another key study in the early stage of this work.
Stennett showed that optimal tracking performance was obtained under
moderate incentive conditions associated with moderate physiological
levels, and that when incentives and physiological levels were extremely
high, performance suffered.
These experiments of Bartoshuk and Stennett (and others to be
described presently) have revealed ANS, somatic, and EEG changes
accompanying performance decrement. Is performance decrement invari-
ably associated with physiological and EEG changes, or is there a kind
of impairment that is not accompanied by such physiological changes?
For instance, Mowrer and his co-workers (Mowrer, 1940; Mowrer,
Rayman, & Bliss, 1940) have shown that divided set, as compared with
single set, generally produces a decrement in performance. Is this decre-
ment to be ascribed to purely cognitive factors, or to factors of high
activation, or to both? This was the question behind a recent unpublished
experiment of mine with forty-two young males in the Royal Canadian
Navy serving as subjects.3 They were trained first to track manually to
auditory stimulation, then to track with their feet to vibratory stimula-
tion on the chest, and finally to combine manual and pedal tracking
(that is, engage in double tracking). After this training, eight experimen-
tal trials were given, with conditions of unified and divided set alter-
nating from trial to trial in a balanced control design. Under the condi-
tion of divided set the subject was instructed to commence manual
tracking, but was told to be ready to shift into double tracking later in the
trial. Under the condition of unified set the subject was informed that
he would not be required to double track on that trial. On divided set
8
The splendid co-operation and very considerable help of these men and of the
Naval Officers who assisted in making the arrangements are gratefully acknowledged.
1963] MECHANISMS IN LEARNING 3
trials the subject commenced double tracking in the last one-third of the
trial. Throughout all trials the following continuous recordings were
taken: EEG (alpha, 8-12 cps, beta, 17-30 cps, and delta, 2-4 cps,
separately filtered and quantified), integrated muscle action potentials
(from forehead, left forearm, right forearm, left leg, and right leg),
heart rate, respiration, palmar conductance, time-off-target, and distance-
off-target. Comparisons between divided and unified sets involved the
first parts of trials, that is, when manual tracking only was being
performed.
Results showed that while the "mental hazard" of having their minds
on two things instead of one increased tracking errors significantly, this
loss in efficiency was not at all reflected in the extensive battery of physio-
logical measures (whose extreme sensitivity was demonstrated by
control conditions in the same experiment). Evidently purely cognitive
factors of set and attention were capable of impairing performance
without affecting the activation (arousal) system.
Interestingly enough, there is evidence suggesting that the impair-
ment on various tasks shown by most schizophrenics may be a phenome-
non nice this, being mainly cognitive (like divided set) rather than
affective in nature. In psychophysiological experiments with chronic
schizophrenics we (Malmo, Shagass, & Smith, 1951) found activation
(arousal) mechanisms relatively intact in the schizophrenics we studied,
although their performance on tasks was grossly impaired. Evidence
for the importance of divided set in schizophrenic impairment is stressed
in a recent review by Shakow (1962) who says:
An examination of the varied aspects of the total portrait I have been presenting,
particularly the trend towards disorganization, reveals that these aspects appear to
involve one or another form of a single but complex type of difficulty. This is the
inability to maintain a major set... .
Although evidences of this difficulty appear throughout our studies, the phenomenon
is perhaps most clearly depicted in the reaction time experiments. Here we see
particularly the various difficulties created by context, the degree to which the
schizophrenic is affected by irrelevant aspects of the stimulus surroundings—inner and
outer—which prevent his focusing on the "to-be-responded-to" stimulus. . . . [The
schizophrenic] apparently cannot free himself from the irrelevant among die numerous
possibilities available for choice (pp. 24-5).
Feldman's (1961) experiment was another study from our laboratory
in which performance (and learning) were significantly affected by con-
ditions that were unaccompanied by any observable shift in ANS
functions. Feldman observed insignificant differences between physio-
logical activity associated with shock-correct (shock intensity constant)
and that associated with shock-wrong, although these two shock con-
ditions had different effects on learning. The sensitivity of Feldman's
4 ROBERT B. MALMO [VoL 17, No. 1
(1961) physiological measures was demonstrated in the same experiment
by their discrimination between electric shocks of different intensities.
Pain, of course, regularly produces sympathetic autonomic reactions in
normal subjects. But painful stimuli that in normal subjects produced
marked autonomic reactions failed to do so in McMurray's (1950) case
of congenital insensitivity to pain, although his pain-free subject showed
quite normal autonomic reactions to changes in task difficulty.
Turning now to other conditions which are activating in normal sub-
jects it has recently been found that increasing drive, by depriving
subjects of food, water, or sleep, regularly produces upward shifts in
physiological levels. In 1959 Belanger and Feldman performed an experi-
ment with rats in which heart rate rose monotonically with hours of water
deprivation and in which, as in Stennett's (1957) experiment, performance
was optimal with moderate levels of heart rate4 and inferior at lower and
higher heart rate values. Performance in the Belanger and Feldman (1962)
experiment was bar-pressing for water. Belanger and his students, in
continuing this line of investigation, are carrying out a beautiful series of
interrelated experiments that is adding significantly to our knowledge of
heart rate (as an index of autonomic nervous system function) in its
correlations with drive and performance (Belanger, 1961; Belanger &
Tetreau, 1961; Ducharme & Belanger, 1961).
Performance under conditions of sleep deprivation produces physio-
logical changes signifying increased activation, and in sleep the direction
of these physiological changes is reversed. Surwillo and I (1960) found
mainly concordant EEG and autonomic shifts to higher activation levels
in sleep-deprived human subjects; and Rust (1962) found monotonically
rising heart rate in sleep-deprived rats. Performance changes in these
experiments were complicated and difficult to interpret, but earlier work
on rats by Bunch, Licklider, and their co-workers (cited in Malmo &
Surwillo, 1960) had demonstrated the beneficial effects of sleep depriva-
tion on water maze learning and performance. Consistent with this
general picture (of rising activation with deprivation and falling activa-
tion with satiation) was the finding of regularly falling curves for various
physiological functions (signifying decreasing activation) during sleep
(Kleitman, 1939, p. 150; Malmo, 1959, p. 380 ff.).
Two other recent studies showing concordant EEC and autonomic
changes are those of MacNeilage (1961) and Pinneo (1961). MacNeilage
^Stennett's (1957) article does not present the heart rate data on which this
statement is based. Stennett's heart rate data were analysed later by R. Elliott, in
two separate analyses. One replicated Stennett's original analysis exactly, and
resulted in very significant inverted U functions within each of his two groups.
Another, very conservative analysis reproduced the inverted U pattern again, but the
reliability of the performance decrement at high heart rate levels was attenuated.
studied a paced serial adding task, finding that task difficulty was re-
flected in the physiological measures, though some of the more compli-
cated aspects of performance appeared not to be closely related to these
measures. Pinneo (1961) found physiological levels monotonically related
to amount of induced tension and he found that induced tension impaired
tracking performance.
To summarize, in addition to the well-known activators such as startling
or painful stimulation and stressful situations, the following conditions
were found to affect autonomic and EEG measures: variations in motiva-
tion, in level of induced tension, and in degree of wakefulness.5 Putting
the behavioural and physiological evidence together it seems reasonable
to consider that a limbic arousal system may play a major role in the
mediation of these autonomic-linked behavioural phenomena.
Among the conditions that were found not to be associated with
changes in autonomic functions were divided set in normal subjects, and
the apparently related phenomenon of inattention in schizophrenics. As far
as neural mediation of these behavioural phenomena is concerned, the
physiological evidence points mainly to cortical mechanisms, whose
facilitation of autonomic effectors is generally much less strong than that
of mechanisms within the limbic system.
Before leaving this topic, I should point out that in the main I have
been dealing with data based on group trends. Unfortunately, it will not
be possible here to deal with other equally important questions concerned
with individual differences that have been investigated so thoroughly in
Lacey's laboratory (Lacey, 1950; Lacey & Lacey, 1958; Lacey & Van
Lehn, 1952) and by others (e.g., the studies of autonomic factor scores by
Wenger & his co-workers, 1957). But it should be mentioned that Schnore
(1959) in following up Lacey's principle of response specificity and some
previous work in our laboratory on symptom specificity in psychiatric
patients (1949) found that during qualitatively and quantitatively dif-
ferent stimulus situations individuals exhibit idiosyncratic but highly
stereotyped patterns of somatic and autonomic activation.
Finally, it should be borne in mind that all of this work was done with
adults. Recently Elliott in our laboratory has been working with children
of kindergarten age, and, from his results thus far, it appears that some
of the relations between performance, incentive, and physiological
measures found in adults will probably turn out differently in children of
this age. Conclusions concerning these age differences must await further
*In an undergraduate research project carried out under the author's direction by
Miss Sylvia Wittkower, reaction time performance was poorer and heart rate and
respiration were lower when subjects were drowsy than under control conditions
when they were more alert.
analyses of his data. But it does seem that Elliott's findings will pose some
difficult questions for activation theory, at least with regard to gauging
levels of drive and motivation by means of peripheral physiological
indicants, and possibly with regard to even more fundamental issues.
Some of these issues have recently been discussed by Irwin (1961,
p. 218), and, as he suggests, the way out of the conflicting theories of
drive is over the rough and winding road of experimentation. As one
who approaches these problems from the neuropsychological point of
view, in my own research I have lately returned to animal experimenta-
tion which provides opportunities for more direct investigation of brain
mechanisms.
In shifting my line of investigation to attack these neuropsychological
problems more directly in animal experiments I was particularly drawn
to an area of research involving ANS functions. I refer to the currently
very active experimentation concerned with behavioural alterations pro-
duced by stimulating or placing lesions in various parts of the limbic
system (Nauta, 1960). Work in this area received a powerful impetus
from the discovery of rewarding areas in the brain by Olds and Milner
(1954) and from the demonstration by Delgado, Roberts, and Miller
(1954) that stimulation in some of these structures in the limbic system
leads to a fear-like reaction with clear drive properties. The limbic system
is known to have considerable influence on autonomic functions.
For example, stimulation in the septal area, one of the rewarding areas
discovered by Olds and Milner (1954), was from Hess* work (1957)
known to produce autonomic changes. In stimulating the septal areas of
anaesthetized cats Hess (1957) had found parasympathetic changes such
as slowing of the heart and lowering of blood pressure which he referred
to as trophotropic responses. From reviewing the work of Hess and others
in relation to his own experiments, Olds (1962) has noted the correlation
of rewarding placements with parasympathetically active points; but he
has repeatedly stated that it is by no means clear that a perfect correlation
exists. He has also pointed out that it is difficult to interpret the available
autonomic data, because most of the autonomic data were recorded from
anaesthetized animals and because generally the autonomic work has been
done on cats, whereas the self-stimulation experiments have been carried
out mainly with rats.
Two years ago, in reviewing the very considerable amount of experi-
mentation generated by the Olds-Milner discovery, it struck me that one
important aspect of the problem had been almost completely neglected.
In the six years of experimentation since the original discovery, there
were (as far as I could determine) no experiments in which autonomic
recordings were taken from animals while they were actually engaged in
self-stimulation and only one study designed to provide information of
any kind concerning what physiological effects these brain stimulations
were actually producing at the time they were being delivered. This one
study was an excellent electroencephalographic experiment by Porter,
Conrad, and Brady (1959) who found in certain monkeys that the occur-
rences of seizures (indicated by the spike and slow-wave complex in the
EECs) appeared essential to intracranial self-stimulation (ICSS). But in
other animals seizures were by no means an invariable accompaniment of
self-stimulation. As Olds (1962) has suggested, those spike and slow-wave
complexes that did appear essential for self-stimulation in certain cases
might prove to be a valuable clue in tracking down the more general
physiological consequences really crucial for the rewarding effects.
I chose heart rate recording as the first step in investigating ANS
reaction during ICSS. There were recording problems at first, but they
were solved chiefly through using a special "noiseless" cable manufactured
by the Microdot Corporation, so that it was possible to record heart rate
even during the half-second periods when the electrical stimulation was
actually taking place. Surgical wound clips were used to attach the
electrocardiograph (EKG) electrodes, one immediately below the heart
on die left side and the other on the right side of the body just back of
the shoulder joint During experimental sessions, continuous tracings of
EKG were taken on a Grass Polygraph.
Experiment I
In die first experiment, using nembutal anaesthesia, I implanted elec-
trodes in the brains of seven young male hooded rats with the intention
of penetrating the septal area. Figure 1 shows a diagram of the electrode
placement in S 5. Below the corpus collosum in the septal area is drawn
the electrode track that was observed in a cresyl-violet-stained brain
section. It will be noted that this section is at the level of the anterior
commissure.
A recovery period of at least three days was allowed after operation
before putting the animal in the testing apparatus. The animal's first
two sessions in the apparatus were for habituation and for training him
to wear the wire attachments to his head and body without biting them.
For the experimental sessions, a lever placed near the floor of the testing
box actuated a microswitch in the Grass stimulating circuit so that by
pressing it the rat received electrical stimulation through the implanted
electrode. Voltage (peak-to-peak) was set initially at 0.8 volts, and was
advanced as required, usually to 3-5 volts. A timer in the circuit cut the
current off after a period of one-half second if the rat continued to hold
the lever down.
ROBERT B. MALMO [VoL 17, No. 1
elcctrocLe.
•t-TCUCK,
ctvLCLatrv, c o r a t i d s s xxca
FIGURE 1. Semidiagrammatic representation of the rat fore-
brain illustrating part of the electrode track as seen in a brain
section from S 5 in the first experiment. The track made by the
stimulating tip of the electrode was in the septal area (see "S"
in the diagram).
Testing sessions in the first experiment were held once a day on five
successive days. Animals were not deprived of food or water during the
experiment. Twenty-minute acquisition sessions were held on the first
four experimental days. In all instances bar-pressing rate had levelled off
before the fifth session. During the first 10 minutes of the fifth session
conditions remained the same: the animals were rewarded with stimula-
tion for bar-pressing. But in the latter half of this (the final) session the
current was turned off so that when the animal pressed the bar there was
no electrical stimulation. This, of course, was the extinction procedure.
Results from this pilot experiment showed that septal stimulation (under
the specific conditions employed) produced significant slowing of the
heart rate (Malmo, 1962, p. 397).
Experiment II
Questions concerning possible artifacts affecting these results can best
be dealt with, I believe, by going on to the second experiment. In most
essential respects the experimental procedure was the same as it was in
the pilot experiment, but, as mentioned, the group was larger. In this
experiment there were 21 animals, and, in addition to heart rate, electro-
encephalograms (EEGs) and respiration were also recorded. There were
five 10-minute acquisition sessions held on consecutive days. In the sixth
session after 5 minutes more of acquisition the current was turned off
and there followed 10 minutes of extinction.
FIGURE 2. Drawing of subject in the free-roving

situation in which bar-pressing was performed.
Compare with Figure 6 for the contrast between
free-roving and restrained conditions. For kind of
head electrode used see text and the drawing in
Olds and Milner (1954).
Figure 2 shows the animal with his attachments on for recording. The
two head electrodes were used for septal stimulation and, between stimu-
lations, for EEC recording from the septal area. The covering, wrapped
around the animal's body (fastened with a piece of strong white tape),
is a strip of soft rubber, cut from a bicycle inner tube. Underneath the
cover are the EKG electrodes and the transducer for recording respira-
tion.6 Figure 3 shows a sketch of this respiratory device that was de-
veloped by Mr. Mundl in our laboratory. The harness of spring brass was
placed on the animal's back, being held there securely by the rubber
*Thanks are due Dr. Willard McFarland for helping us to solve some of our
problems associated with recording respiration, and also with restraining rats
(infra, 17-18).
Rtspiroiton
Trantductr
RuhfrBMog
FIGURE 3. Diagram showing arrangement for recording respira-

tion in the rat. Respiration is recorded by means of two strain
gauges, one at the top of the arch and one just below it. The three
wires shown are attached as follows: (a) to one terminal of the
upper strain gauge, (b) to one terminal of the lower strain gauge,
and (c) joining the two remaining terminals, one from each
strain gauge.
wrapping. Two strain gauges were cemented to the arched portion of the
harness, one on the upper surface and the other on the lower surface, such
that the lower strain gauge was stretched with inspiration and the upper
one was compressed (the converse relation holding for expiration). From
the two strain gauges flexible lead wire was led to the recording
apparatus.
The tracings in Figure 4 were taken from S 17 whose style of bar-
pressing was particularly well suited to physiological recording. Typically,
he would adopt a reclining position with his body shifted over on the
right side, partly supported by the right paw, and with the left paw
resting on the bar. Without moving from this position the animal could
easily stimulate his brain at any time he pleased. Since the stimulus cut
off automatically at the end of one-half second, there was no danger of
overstimulation from his resting on the bar in this way; and when the
animal wanted another stimulation all he had to do was to raise his left
paw off the bar momentarily and come down to rest on it again, the
weight of his arm holding the bar down without effort
The figure shows two bar-presses (two sequences of this cyclic be-
haviour). Note the shift from slow to faster heart rate as the animal
rested on the bar, with the fastest heart rate appearing at the very end
of the bar-presses before the animal went into action to stimulate himself
again. This change is easier to see in the electrocardiotachogram (ECTG)
(the longer the ECTG deflection, the slower the heart rate). Commencing
1963] MECHANISMS I N L E A R N I N G 11
INTRACRANIAL SELF-STIMULATION
KG ', 150 ^v
16-28cps
Integrated EEG
l l | l I I I I I I I H I H I 1 l l l l l l l l l l l ) I I I H I I I I ! t l l H I H I H ) l r ) l - l i l l l l l l ' . l i l ' H I l l l l l l ! II I I I H i l l
EKG
f-*m Brain Him. Bar-prate g g ^ _ Brain slim.
FIGURE 4. Physiological tracings recorded during septal self-stimulation in S 17.

Note especially the rise in heart rate (indicated by the shorter ECTG deflections)
which immediately preceded self-stimulation. The extremely short ECTG deflections
coinciding with brain stimulation are artifacts produced by the stimulating current.
Note that EEG artifact was also due to stimulating current and not to the subject's
movements.
with stimulation and for about two seconds afterwards, the ECTG, is lost
through switching artifact. But the electrocardiogram (EKG), which is
recorded without artifact, shows the gross heart rate slowing during this
immediate post-stimulation period. The absence of spike and slow-wave
activity in the EEG can also be observed. Some of the bar-presses were
quite long. Figure 5 shows one that lasted about 15 seconds. Again there
was the gradual change from slow to faster heart rate during rest.
From the evidence there seems little doubt that septal stimulation
produced the cardiac slowing directly, that is, without the mediation of
skeletal activity. In twenty animals taught to lie quietly in our restraining
device (see Figure 6) there was a mean heart rate decrease of 24.3 per
cent upon stimulation. This finding was based on 10 stimulations per day
over a period of 12 days. This amount of heart rate change is of the same
order as the amount of acceleratory change observed in animals actually
performing a motor task (e.g., mounting a platform; see McCleary,
1954). Moreover, the heart rate decelerations with septal stimulation
were about twice as great on the average as the largest decelerations
observed (by D. J. Ehrlich and myself in another experiment) in certain
INTRACRANIAL SELF-STIMULATION
EEG \so/N
30 - 50 cps
16 - 28 cps
Integrated EEG
Respiration
Mnmiiiniim
EK6
-*— Brain stint. Bar-presi
FIGURE 5. Physiological tracings recorded during septal self-stimulation in S 17

during a long bar-press. Note especially the gradual rise in heart rate indicated by
the gradual shortening of the ECTG deflections. Note that the EEG artifact was due
to the stimulating current and not to the subject's movements.
rats that early in learning to bar-press for food showed heart rate slowing
in a high proportion of trials. Moreover, the septal stimulations continued
to produce heart rate slowing without any habituation over the period of
12 days, whereas receiving pellets in the bar-pressing situation was not
a condition that continued to produce consistent heart rate decelerations
after the first session or two. Considering the fact that the heart rate
decelerations with septal stimulation were of the same order as heart
rate changes observed in rats actually performing overt acts requiring
physical exertion, and that they were significantly more pronounced than
changes associated with bar-pressing for food, they could scarcely have
been artifacts due to some kind of postural adjustment (such as assuming
a tense vigilant posture or the like) that was invisible to the observers
and undetected by die sensitive recording devices.
Was heart rate slowing to septal stimulation secondary to respiratory
change? In the physiological laboratory, acceleration of heart rate during
inspiration and deceleration of heart rate during expiration are fre-
quently observed. This phenomenon, called respiratory sinus arrhythmia,
has recently been studied by Westcott and Huttenlocher (1961) in con-
nection with cardiac conditioning experiments with human subjects. It is
clear that a single sharp inspiration is usually accompanied by an initial
rise, followed by a fall in heart rate (as illustrated in their Figure 2,
p. 355). With regard to my experiment, if brain stimulation had regularly
produced such a sharp inspiration, heart rate slowing would have been
expected, following initial heart rate acceleration, and the heart rate
reaction would then be accurately described as secondary to the respira-
tory reaction. As Figures 4, 5, 7, and 9 demonstrate, however, no abrupt
respiratory change of this kind was required for very marked heart rate
slowing to appear following septal stimulation. Still, as is clear from
Figure 9, septal stimulation did produce some definite changes in respira-
tion; and, as in the Figure 9 tracing, the altered respiration tracing
generally had a very regular appearance. It is not surprising that septal
stimulation, in addition to slowing the heart rate, should have such effects
on respiration. Stimulation at this forebrain level, as Hess (1957) showed,
produces multiple autonomic effects. In Hess' writings there is no
suggestion of heart rate slowing being a secondary reaction. He called
particular attention to the reduction in heart rate that he regularly found
in stimulating certain parts of the brain, stating that in many stimulation
points (especially in the septal area) the reduction in heart rate was
accompanied, for example, by a drop in blood pressure.
Granted the heart rate slowing in my experiment was not caused by
some irregular break in the respiratory pattern, such as a sudden deep
inspiration, is there any possible way that the heart rate slowing could
have been produced as a reaction secondary to the respiratory changes
that were observed? To make this question more concrete, assuming
Clynes (1960) is correct, heart rate arrhythmia that is secondary to
breathing is initiated by stretch receptors in the thorax. It is conceivable,
though unlikely, that a relatively slight change in the respiratory pattern,
such as the one shown in Figure 9, could slow the heart by means of
Clynes' stretch reflex. If the effect of septal stimulation on respiration
were as consistent as its effect on heart rate, it would be difficult to rule
out such a possibility. But, as it turned out, the respiratory effects of
septal stimulation were actually quite variable from subject to subject
although quite consistent within subjects.
Careful measurements of rate and amplitude have been completed for
11 septal animals and the breakdown for mean changes with septal
stimulation is as follows. Two animals (including S 18 whose tracing is
presented in Figure 9) showed decreased rate and amplitude, three
animals who also showed decreased rate showed increased amplitude.
But 6 of the 11 subjects showed an increase in rate: in 5, combined with
a significant decrease in amplitude, and in one with no significant change
in amplitude. Except for this one animal with insignificant change in
amplitude all mean changes in rate and amplitude were statistically
reliable. Despite these widely varying interindividual differences in pat-
tern of respiratory change, all 11 animals showed highly significant heart
rate slowing with septal stimulation. From these data it appears safe to
conclude that the heart rate changes were not secondary to some
peripheral respiratory effect such as changes in thorax circumference
acceleration.
It is important to note, by the way, that the combination of increased
rate and increased amplitude of respiration did not appear even once in
the group of 11 septal animals for which measurements were available.
According to Kabat (1936) "spitting in cats, a mimetic response simulat-
ing intense emotion," has been found to occur only during stimulation of
certain sharply localized regions of the brain (never the septal area);
and this reaction was practically always associated with a marked increase
in respiratory amplitude and often with an increase in rate. In short, in
the cat the combination of increased rate and amplitude appears clearly
to be a sympathetic reaction, and it is very interesting that of all the
various combinations observed with septal stimulation, this one was not
observed.
It may be asked whether the observed parasympathetic reactions to
septal stimulation (also observed by Hess, 1957) were secondarily in-
duced by preceding sympathetic reactions. This is a question concerning
mechanisms of autonomic balance, the subject of a classical paper by
Darrow (1943). The subject of cardiovascular homeostatic mechanisms
has more recently been thoroughly discussed by Lacey (1956) who points
out that with direct stimulation of vagus and cardiac sympathetic
accelerator nerves the vagal effect is far more prompt than the accelera-
tory effect (Lacey, 1956, p. 129). The very short latencies of the heart
rate slowing reactions observed in my experiments, and the fact that the
tracings did not show heart rate acceleration immediately following
septal stimulation, seem to rule out the possibility that these parasympa-
thetic reactions were compensatory (i.e., reactions to initial sympathetic
response).
Note the absence of spike and slow-wave (that is, "seizure") patterns in
the EEG associated with septal stimulation. There was abundant evidence
in this group of animals that heart rate slowing could occur in the
absence of this "seizure" pattern in the EEG. In connection with this
evidence, it is of interest to note the statement by Penfield and Jasper
(1954) that petit mat attacks seem not to be regularly associated with
cardiac slowing.
Heart rate change produced by stimulation was determined by sub-
tracting the post-stimulation heart rate (for a two-second period com-
mencing one second after onset of stimulation) from a four-second
pre-stimulation heart rate. Because it was essential that brain stimulations
be spaced far enough apart to provide a valid measure of pre-stimulation
heart rate, brain stimulations that were less than 8 seconds apart were
not used in the heart rate analysis. For S 17, 67 computations of heart
rate change could be made, and they were all in the direction of heart
rate slowing. The consistency of heart rate fall with brain stimulation for
the group of 21 animals was extremely high. Without exception the mean
heart rate change was in the direction of slowing, the * being 8.8. The
heart rate slowing reaction to septal stimulation was so definite, pre-
dictable, and persistent, stimulus after stimulus, day after day, and animal
after animal, that it was possible to pair this response with a tone and to
condition it so that eventually the tone alone would elicit it. The con-
ditioning experiment will be presented in detail later in this paper. Here,
if I may impose divided set on you by bringing the conditioning experi-
ment into this discussion, I wish to mention some incidental observations
(drawn from both experiments) that revealed the decisive importance of
the animal's ongoing behaviour in determining the effects produced by
brain stimulation. We are dealing now with general questions, not with
specific points related to conditioning mechanisms; and hence detailed
information concerning the conditioning experiment is not required here.
Compare Figures 2 and 6. In bar-pressing (see Figure 2) the animal
was free to move about and he produced his own brain stimulations by
pressing on the bar. On the other hand, in the conditioning situation
(see Figure 6) he was lying in a hammock wrapped about with rubber,
having learned not to struggle, passively accepting the situation in which
brain stimulations preceded by tones were administered by the experi-
menter at intervals of approximately 30 seconds. Nineteen animals were
observed under these two conditions of passive and active brain
stimulation.
Now when the rat is free from any such restraint, just moving about
the cage, often the effect of electric shock, as anyone who has ever
shocked rats knows, is to make the rat stand still (or to "freeze"). But
from our observations the reaction of a restrained animal to even a mild
electric shock is quite different. During these pilot studies, on a few
occasions, we noted the after-effect of a mild electric shock on the
restrained animals, and in every instance shocking their feet initiated
violent struggling which continued with such force after the shock that
the restraint had to be removed. Stimulating animals' septal areas,
however, never produced such reactions. As a matter of fact, septal
FIGURE 6. Drawing of subject in the restraining device

used in the heart rate conditioning experiment. Compare
with Figure 2. See text for description of procedure in
heart rate conditioning experiment.
stimulation seemed helpful in getting the animals to lie quietly. This

observation, it may be noted, seems inconsistent with the fact that in
pressing the bar for brain stimulation some animals appear very excited
at times. Why is it that septal stimulation produces this apparent excite-
ment in the active bar-pressing situation when it fails to do so in the
restrained animal passively accepting septal stimulation from the experi-
menter? I don't know the answer to this question. But the very existence
of the problem shows how unsatisfactory it generally is to specify the
effect of stimulating a particular place in the brain, without regard to the
animal's behaviour prior to stimulation.
Some behavioural observations from the extinction condition of the
self-stimualtion experiment are relevant here. Figure 7 shows the tracing
for S 17 at the transition point between acquisition and extinction. The
current had just been turned off. Following the final brain stimulation
with heart rate slowing, there was again the gradual return to faster
heart rates during the typically long bar-pressure (see Figures 4 and 5).
But observe the radical change in pressing pattern when the animal's next
pressure failed to produce brain stimulation. Before the stimulating cur-
rent was turned off, that is before the extinction condition, behaviour
EXTINCTION OF INTRACRANIAL SELF-STIMULATION
16 - 28 cps 120 pv
Integrated EEG
Respiration
lllluJhlH
EKG
Bar-presses without brain stim.
ECTG
FIGURE 7. Physiological tracings from S 17 recorded during intracranial self-stimu-
lation in first part of extinction, immediately after stimulating current had been
turned off. Note especially the repetitive bursts of pressing (atypical for this animal
during the acquisition phase); and also note the signs of disturbance in the physio-
logical tracings: movement artifacts in the EEC (current was off so that artifacts
were not produced by stimulating current as previously), gross irregularity of the
pneumograph tracing, and appearance of muscle potential artifacts in EKG not
present in any of the other four Figures (4, 5, 8, and 9) showing EKC tracings.
was extremely well controlled—almost machine-like. But, after the current

was turned off, on the first bar-press that was not followed by stimulation
this behaviour pattern was instantly disrupted and the picture was
changed to one of marked motor excitement. Watching the animal we
had Sie distinct impression of seeing the "terrible-tempered Mr. Bang"
in action. The greatly heightened motor activity (apparently an exag-
geration of the increased responding sometimes observed at the beginning
of extinction) is reflected in the movement artifacts that completely
obliterated the EEG tracing from the beginning of extinction, and in the
muscle potentials appearing in the EKG tracings (see Figure 7).
While I have presented data for only one animal, this is by no means
an isolated instance. On the contrary, it seems particularly characteristic
of animals that have had a regular pressing pattern of this kind to show
disorganized and excited behaviour during the first part of extinction.
This looks like frustration of the kind that Amsel and his co-workers
(Amsel, 1962; Amsel & Roussel, 1952) have shown to be energizing. I am
not refuting any of Amsel's arguments in the discussion that follows. But
the problem becomes still more complicated when we look again at the
results from the conditioning experiments.
The tracings in Figure 8 are from the same animal whose disturbed
record we just saw. After 120 pairings of tone and septal stimulation,
enough to produce conditioning of heart rate slowing, the tone was pre-
sented alone without brain stimulation on the first extinction trial. If the
septal stimulation, regularly administered to the animal following tone,
were indeed a positive ("rewarding," "pleasurable") stimulus, it seems
not unreasonable that the animal might build up the expectancy: brain
FIRST EXTINCTION TRIAL
J50*iV EEG
3O-5Ocpi
—V—'~L-—L
16
Integrated EEG " 2 8 cps
Respiration
Hiiiniiiiniii 111 u i n n i nun
EKG
Tons without brain stint.
ECTG
FIGURE 8. Physiological tracings recorded during first extinction trial in classical

heart rate conditioning with S 17 in restraining device. Note the conditioned heart
rate slowing on this test trial after 24 hours without brain stimulation, and note also
the absence of movement artifacts in the tracings. For S 17 the same stimulating
voltage was used in classical conditioning and in ICSS.
stimulation regularly follows tone. In Mowrer's terms, the tone might
come to elicit "hope" (Mowrer, 1960, p. 59) and, again according to
Mowrer (1960, p. 165), one possible result of extinction under these
circumstances might be "anger." But watching this animal and each of
the others, at the time he received his first CS without brain stimulation,
failed to reveal any sign of activation due to omitting brain stimulation.
The fact that the animals were restrained in the classical conditioning
situation is, of course, to be kept in mind, but there was nothing about
the restraint that would have prevented the appearance of artifacts in
EEG and respiration tracings, artifacts like those in Figure 7 for the same
animal (S 17) during extinction in the instrumental conditioning situa-
tion. But as can be seen in Figure 8, no such artifacts appeared on the
first extinction trial in the classical conditioning situation. The conditioned
heart rate slowing is clearly visible, but in the tracings nothing new
appeared that could be interpreted as evidence of even the slightest
emotional disturbance. Ratings of artifacts in the records for the entire
group of animals indicated that this difference between conditions
observed in the tracings of S 17 was a representative one. The two raters
who were not informed concerning the purpose of the analysis yielded
data that showed a statistically reliable increase of movement artifacts
at the beginning of extinction in instrumental learning, without a corre-
sponding significant increase of artifacts in the first trial of the classical
extinction.
In the passive ( classical conditioning) situation it were as though "hope"
was not aroused by the tone, or, if it was aroused, that "anger" failed to
occur, when in extinction the tone was not followed by septal stimula-
tion. Anthropomorphically considered, it were as if having exerted no
effort to obtain the septal stimulation the animal had not earned the right
to object to its omission! Seriously though, it would appear that the
animal's bar-pressing response in producing the brain stimulation (and
the proprioceptive feedback) was essential for the appearance of the
expectancy-frustration phenomena. There is a certain resemblance to the
finding of Brady, Porter, Conrad, and Mason (1958) that it was the
"executive" monkey and not the control monkey that developed ulcers in
a situation where the "executive" was required to press a lever regularly
to avoid shock for himself and for his passive partner, the control monkey.
Of course, theirs was a controlled experiment focused on the active-
passive comparison, while our observations on this point were incidental
ones. Our findings also appear related to Teuber's concept of corollary
discharge as applied to the observations in perceptual rearrangement
experiments that "reafferent" stimulation (actively produced by the
perceiver) is prerequisite for adaptation (Teuber, 1960, p. 1636).
All of this raises some fundamental questions concerning the concept
of expectancy itself (e.g., its neural mediation) and its place in the
context of conditioning and learning. Apparently brain activities such as
those mediating the motor sequences in bar-pressing (plus the various
related feedback circuits and neural associative mechanisms) are re-
quired for the development of observable expectancy reactions. This
seems to be very much the same point that Smith (1954) is making in
the final paragraph of his paper.
On the other hand, the conditioned heart rate slowing I obtained, in
the absence of skeletal-motor accompaniments, appears to refute Smith's
arguments that conditioning is an artifact and that ANS responses cannot
be conditioned. If it is argued that my experiment is not a refutation of
this position because there may have been some skeletal reactions too
small to be detected even by our sensitive recorders (see Smith, 1954,
p. 223), I would reply that in certain animals the magnitude of the heart
rate CRs was beyond the range where such an explanation could validly
be applied; (the question of interrelations between heart rate and respira-
tion will be dealt with later). Four animals showed mean heart rate
decreases of more than 9 per cent for the last session of conditioning; and
the peak CRs for each of these same four animals (again for the last
session) were as follows: 24.30 per cent, 19.78 per cent, 19.06 per cent,
and 21.67 per cent. As previously explained, reactions of this magnitude
are of the same order as reactions accompanying overt activity involving
appreciable exertion. Furthermore, it should be stressed that these CRs
are heart rate decelerations. It should be recalled, moreover, that accord-
ing to Razran (1956, p. 50) Smith has ignored important Russian experi-
ments that make his position indefensible.
Problem of Neural Mediation of Reward

In returning to the more physiological side of the problem now, it is
clear that the behavioural aspects of the experiments must constantly be
kept in mind. We have just observed how meaningless it is to specify the
effects of brain stimulation without regard to the animal's behaviour
immediately prior to stimulation. It was clear, for example, that septal
stimulation did not generate excitement in restrained animals. The data
suggested, by the way, that excitement, when it did occur during ICSS,
was probably more closely connected with disappearance of the effects
produced by stimuation than with onset of stimulation; although it would,
of course, be premature to conclude that the "angry" excitement observed
in extinction of bar-pressing is the same kind of excitement that is some-
times observed during ICSS (with the current on). Finally, as will be
clear as the discussion proceeds, I believe it is also premature to draw
too strong a line between the ANS changes accompanying septal stimula-
tion and the reinforcement mechanisms mediating ICSS.
Olds, himself (1962), has recently turned away from the idea of a
one-to-one linkage between parasympathetic autonomic responses and
appetitive reactions. On one hand he says: "a large system of the brain
phylogenetically derived from the olfactory apparatus and possibly still
specialized to chemoreception apparently functions primarily to mediate
conservative and appetitive reactions. The former are uncovered by
observing the autonomic responses produced by electric stimulation in
these areas, the latter by observing instrumental or consummately re-
sponses yielded by the same stimulation" (Olds, 1962, p. 592). But in
another place he says:
Some tendency of parasympathetic-like responses to be found in areas associated
with positive reinforcement and sympathetic-like responses to be found in areas asso-
ciated with negative reinforcement is suggested. However, it is by no means clear that
a perfect correlation exists. That there should be mixed autonomic responses from a
drive-reward system is reasonable considering the widely variable nature of the
instrumental-and-then-consummatory behavior series involved (Olds, 1962, p. 579ff.).
As Olds goes on to say, the main problem, of course, is to understand
the neural mechanisms mediating these appetitive and autonomic reac-
tions. This problem is not likely to be solved very soon. In the meantime,
however, frankly speculative notions are potentially useful in stimulating
experiments that might help in the eventual solution of this problem,
and Olds* recent (1962) speculations are of interest from this point of
view. Olds* notion is that "the main substrate of reward is a set of granule
cells which forms a system through the lateral hypothalamus, basal
ganglia, and paleocortex." He suggests as one possibility that the reward-
ing effects from tongue or genital receptors may perhaps be produced by
a process of double inhibition. As I understand his idea, impulses from
the periphery fire reinforcing paleocortical areas, such as the entorhinal
one, which in turn inhibit die cells of the dorsal reticular formation or
medial hypothalamus. These dorsal recticular formation or medial hypo-
thalamic cells are the inhibitors of the granule cells. (Results from Olds'
experiments with animals self-injecting their brains with chemical sub-
stances—cited in Olds, 1962—suggested the possibility that the granule
cells do not have excitatory afferents but instead have high rates of
spontaneous activity.)
If I may be permitted to engage in a little dramatization based on the
one-reelers of 50 years ago, the inhibitors of the granule cells are the
villains, always stirring things up, interfering with the granule cells. The
heroes of the piece come into action to stop this interference with the good
work of the granule cells.
One of the villains appears to be located in the dorsomedial tegmentum.
Stimulation there is noxious as Olds and Peretz (1960) have demon-
strated with escape tests. They also found low EEG arousal thresholds
in these animals, further evidence for the general activating nature of the
tegmental stimulation. There is also evidence that stimulation in this
region produces autonomic activation. Stimulating in this midbrain area,
McQueen, Browne, and Walker (1954) found blood pressure rise accom-
panying EEG arousal. Although the influence of midbrain mechanisms
on cardiovascular functions has not been extensively investigated, as
Oberholzer (1960) and Uvnas (1960) have pointed out in recent reviews,
there is good evidence that these blood pressure rises did not merely
result from activation of descending fibres of hypothalamic or other fore-
brain origin, but were actually due to stimulation of mechanisms located
in the midbrain itself.
This view is supported by the physiological and behavioural evidence
of Bard (1960) and by anatomical evidence recently summarized by
Nauta (1960). According to Nauta the fibre groups in question all appear
to articulate with the midbrain reticular formation and there is good
evidence that the stimulus transmission involves most of the cross-section
of the brain stem tegmentum and the central gray substance. To the best
of my knowledge no one has made any autonomic recordings in animals
during escape or avoidance situations involving tegmental stimulation.
Miss Lucy Gardner in our laboratory has commenced an experiment
along these lines.
If, as Olds (1962) suggests, the negative reinforcement is due to
inhibition of the granule cells, and if this inhibition were itself inhibited,
as previously explained, positive reinforcement should result There is
evidence to support this. Stimulation in the entorhinal paleocortex (one
of the rewarding areas) has been found by Adey (1958) to inhibit the
single cell responses in the dorsomedial tegmentum. Now if tegmental
activity shifts the autonomic balance in the sympathetic direction, inhibi-
tion of tegmental activity should produce a shift in the opposite (para-
sympathetic) direction. The heart rate slowing in my experiments could
have been produced in this way, at least in part.
As is well known, changes in heart rate during normal activity involve
adjustment of the balance between the effects of two sets of autonomic
nerves, vagal and sympathetic. If stimulating electrodes are placed on
the vagal and sympathetic nerves leading to the heart, the heart rate can
be altered to any desired level merely by adjusting the frequency of
stimulation applied to one or both nerves. In the same way normal adjust-
ments in the heart rate can be effected through reciprocal innervation in
the central nervous system, since heart rate can be slowed by an Increase
in the vagal discharge frequency, by a reduction in sympathetic activity,
or by both in combination. To repeat, the heart rate slowing could be
accounted for by inhibitory impulses from some area like the septum
blocking sympathetic discharge from the limbic midbrain area. There
are fibre connections between the septal area and the midbrain (although
it is not known whether these impulses from the septal area are inhibitory
or excitatory). If it turns out that the influence is mainly inhibitory, the
autonomic data would fit in very neatly with Olds* (1962) schema if
inhibition of this midbrain area were to slow the heart at the same time
as it increased the activity of the granule cells.
From heart rate investigations with self-stimulating animals deprived
of vagal influence on the heart (by atropine injection or vagal section),
it should be clearer whether the heart rate slowing is due to sympathetic
inhibition, to pure vagal stimulation, or due to some mixture of the two
effects. The promptness and magnitude of the slowing reaction seem
more in keeping perhaps with some kind of direct vagal stimulation. But
this is a matter for further experiments to decide.
Also planned are experiments in which autonomic and EEG recordings
will be taken from animals self-stimulating in rewarding areas other than
the septum. From physiological experiments (Gloor, 1954, p. 779) it
would appear that posterior hypothalamic self-stimulation (which is re-
warding) might well be accompanied by sympathetic autonomic changes.
But again, this is a question that must be put to experimental test by
making physiological recordings during the actual bar-pressing.
In summary, the autonomic nervous system is definitely tied in with
this whole intricate neural network underlying reinforcement; and
information concerning changes in the autonomic nervous system under
all the different conditions of positive and negative reinforcement should
be invaluable in working towards a clearer understanding of reinforce-
ment mechanisms. Combined with behavioural observations and electrical
recordings from the brain, the peripheral autonomic changes, in reflecting
activity in central mechanisms upstream, may help reveal the neural
mechanisms that are essential for reinforcement.
Conditioning of a Centrally Elicited ANS Response (in the Absence of

Reward)7
My final topic concerns the conditioning experiment that I mentioned
earlier. A quarter century ago in some brilliant pioneering experiments
Loucks (1935) attempted to condition leg movement to a buzzer with
7
Some readers may be confused by my reference to conditioning (or learning)
in the absence of reward. For the context in which I am using these terms see
Kimble(1961,p. 214).
direct stimulation of the motor area in the brain as the unconditioned
stimulus (US). He failed to establish a conditioned response (CR) of
the leg in any one of the three dogs receiving approximately 600 trials
each. But lifting of the leg to brain stimulation was an adequate basis
for conditioning if each movement was rewarded with food. These experi-
ments were widely cited as evidence that conditioning in the absence of
reward was impossible when the unconditioned stimulus was direct
stimulation of the brain.
However, on the basis of later experiments by Brogden and Gantt
(1942) and some much more recent ones initiated by Ciurgea and
continued by Doty and Giurgea (1961), it now appears possible, though
not easy, to condition animals (without reward) when the unconditioned
response (UR) is elicited by direct stimulation of the brain. Brogden and
Gantt (1942) reported conditioning 8 dogs, with 6 dogs showing a high
degree of similarity between CR and UR when the US was stimulation
of the cerebellum and the UR skeletal movements. For example, in one
of the two best conditioners, the US evoked a clear-cut, discrete flexion
of the ipsilateral foreleg, and the CR was almost an exact duplicate of
the UR. In two dogs, however, the CR and UR were dissimilar.
Doty and Giurgea reported successful conditioning, employing pro-
cedures essentially similar to those that had failed to produce condition-
ing in Loucks' experiments. This investigation was a replication of the
conditioning experiments that Giurgea had initiated in Bucharest. In
three of four dogs the CR and UR were similar, from the beginning of
conditioning. In the fourth dog the CR appeared initially in the "wrong"
leg, but in subsequent trials the CR shifted to the same leg that was
lifted to the unconditioned stimulus. In two monkeys there was a high
degree of similarity between CR and UR. In attempting to account for
their success and Loucks' failure to produce conditioning in the absence
of reward, Doty and Giurgea stressed the importance of the intertrial
interval. Loucks used intervals of two minutes or less whereas an inter-
trial interval of three to five minutes was used in the experiments of
Doty and Giurgea. In earlier experiments Giurgea had found that if the
intertrial interval were reduced to two minutes even after CRs had been
established, the CRs disappeared in the majority of dogs tested although
the URs were unaffected.
On the basis of these more recent experiments, then, it appeared
possible, though not easy, to condition animals (without reward) when
the US was direct stimulation of motor cortex. In their behavioural de-
scriptions, Doty and Giurgea present convincing circumstantial evidence
for the absence of motivation in these conditioning procedures. They
stressed the fact that the conditioned movements were non-purposeful,
calling them physiological absurdities. For example, they say (p. 146),
"Watching Monkey I day after day raise its arm to stimulation of its
'visual' cortex one could not escape the feeling that this nonsensical yet
persistent movement was somehow analogous to the compulsive move-
ments of neurotic humans."
In his (1943) book Masserman described his attempts to produce
autonomic conditioning. In some preliminary experiments carried out
with lightly anaesthetized cats Masserman presented a three-second
sensory stimulus (for example, a loud sound combined with an intense
light) as CS followed by the US, direct stimulation of the hypothalamus.
URs produced by hypothalamic stimulation were pupillary dilation, erec-
tion of the hair, clawing and running movements, and blood pressure and
respiration changes. In four animals CS and US were paired 140 or more
times over a period of five hours without producing conditioning. It
seems possible that the anaesthesia may have prevented conditioning
because in later experiments with implanted electrodes in unanaesthetized
animals six subjects showed a "slight [conditioned] pupillary dilatation
and a transient startle or crouching response" to the sensory stimulation
after from 80 to 160 conditioning trials (see p. 43). These positive find-
ings of Masserman's are rarely mentioned in reviews probably because
the CRs were inconstant and lacked the apparent emotional intensity
that is expected when cats are threatened with a dangerous situation.
His negative findings with 18 animals have been widely cited in connec-
tion with those of Loucks (1935).
To the best of my knowledge there have been relatively few reports of
classical conditioning experiments with intracranial brain stimulation as
the US and with some ANS reaction as the UR. Ban and Shinoda (1956)
at Osaka University reported conditioning in two animals. In one animal,
using sparking sounds from an inductorium as the CS and stimulation of
the ventromedial hypothalamic nucleus (which produced sympathetic
autonomic changes) as the US, they were successful in obtaining con-
ditioned pupillary dilation. But results from the other animal in which
the US (stimulation in the lateral hypothalamic nucleus) produced the
parasympathetic response of pupillary constriction failed to show con-
ditioned pupillary constriction. Instead, the CS regularly produced a
slight change in the opposite direction (i.e., slight dilation). In the
same experiments, results appeared to show respiratory and gastric con-
ditioning in the same two animals, but because these data were not
presented in detail, it is difficult to judge them.
Since 1956 these two workers have published two more papers report-
ing conditioning experiments with hypothalamic stimulation as US and
the following measures as indices of autonomic URs: gastric motility
(Ban & Shinoda, 1960); blood sugar level and leucocyte count (Shinoda
& Ban, 1961). In these later experiments they reported sympathetic gastric
conditioning, but once more they encountered reversal in parasympathetic
conditioning when one of their two animals showed an increase in blood
sugar level to the conditioned stimulus, again, contrary to the direction of
change (decrease in level) that was produced by the brain stimulation.
It was the relative paucity of information concerning autonomic nervous
system conditionability, particularly on the parasympathetic side, that
made it seem worth while to try conditioning the septal heart rate slowing
reaction that I described earlier. I implanted electrodes in the brains of
twenty naive male hooded rats, whose median preoperative weight fol-
lowing 24-hour fast was 240 gm. We allowed a recovery period of at
least three days before training the animals to accept restraint, and at
least seven weeks before commencing any experimental testing.
The conditioned stimulus, a 4000 cps tone, presented by a Heathkit
audiogenerator through a speaker 3 feet above the animal, was 65 db
above normal human threshold (as determined by a Maico audiometer).
Through the same speaker ASA white noise (approximately 45 db above
threshold) from a Scott random noise generator was constantly present,
serving as a sound screen. The animal's restraining stand was located
inside a tall steel cabinet that served to protect the animal from visual
distractions. The experimenter could view the animal through a mirror.
Intervals between tone presentations ranged from 20 to 40 seconds in
5-second steps, and were presented in a random sequence in order to
avoid temporal conditioning. In each 6-minute daily session there were
10 trials.
There was no significant unconditioned heart rate response to tone.
The mean response for the group on the 10 tonal stimulations in the
first session was very slightly in the direction of heart rate acceleration
(one-third beat per minute). The other sessions with tone alone (prior
to conditioning) yielded mean changes that were not significantly dif-
ferent from this. But to be certain that the animals were thoroughly
habituated to the tone before conditioning, each animal received at least
80 stimulations with tone alone.
In presenting the unconditioned stimulus a hand switch used in con-
junction with a Hunter timer set for % second produced stimulation that
was delivered by a Grass Model S4 stimulator set for biphasic electrical
stimulation with a duration of 0.5 msec, and a frequency of 100 cps.
Voltages, selected for each animal individually to produce a visible
change in heart rate (without overstimulation), ranged from 5 to 10.5
volts peak-to-peak. Mean unconditioned heart rate slowing for the group
was 99 beats per minute.
Paired stimulations in conditioning were presented as follows. An
automatically timed stimulating circuit was used in presenting the follow-
ing sequence of stimuli: tone on alone for 3 seconds, followed by tone
and brain stimulation on together for the next % second, then both off
(see Figure 9). Ten trials of paired stimulations were given in daily
6-minute sessions for 12 days so that each animal received 120 acquisition
trials. Note that the average interstimulus interval of approximately 30
seconds justifies our regarding the trials as being "massed." I decided,
nevertheless, to risk whatever inhibitory effects might result from massing
in order to obtain what I thought would be a sufficiently large number
of trials in each 6-minute daily session. Some animals would not accept
restraint for a longer period.
Following acquisition, nine extinction sessions were given, i.e., tone
<WMl"*^M^(/V\^V^^
EEG
30 - 50 cps
Integrated EEG 16 - 28 cps
wwv^v\/vvvwvvvvv\^^
Respiration
+444- I K I - H i n
EKG
Tone " ^ Brain Stim.+Tone
FIGURE 9. Physiological tracings recorded during heart rate conditioning. Note

that there are nearly 5 seconds of tracing preceding tonal stimulation (the "pre"
period). "During" period is the 2-second period immediately preceding brain
stimulation. Arrow shows onset of brain stimulation. Tone continues with the brain
stimulation for the X second indicated by the thickened line.
without brain stimulation, ten trials per session, 90 trials in all. Finally,
in a free situation over a period of six days the animals were trained to
self-stimulate. At the conclusion of the experiments the animals were
sacrificed and the electrode tracks were verified histologically.
Figure 10 presents three photomicrographs showing part of the series
of cresyl-violet-stained frozen sections from the brain of S 20. The
middle photomicrograph shows the actual location of the electrode tip,
the top one shows a section slightly anterior to the tip (note penetration
through the corpus callosum), and the lower photomicrograph shows an
intact section slightly posterior to that of the electrode tip. All sections
are at the level of the rostral part of the anterior commissure. This
placement is typical for the series of experimental animals.
Direct evidence that the electrodes were in a "rewarding area" was
obtained at the conclusion of the conditioning experiment, when the
animals were trained to self-stimulate. Late in training the mean bar-
pressing rate for this group was 11.02 presses per minute, well above the
operant rate (usually below one press per minute) for a box of this kind.
The results of the conditioning experiment were positive. Figure 11
shows the acquisition and extinction curves for the group of animals.
These trends were reliable statistically. The acquisition curve is based on
an N of 20 and the extinction curve on an N of 17 (3 Ss could not be
included because of numerous artifacts in their records). The value
plotted in the graph is based on a difference score which is readily
understood by referring to the photograph of a tracing in Figure 9. The
time line on the tracing is marked off in one-second intervals. On the
section of tracing shown in Figure 9 there are nearly 5 seconds of tracing
prior to onset of tone. The heart rate during the 5-second period pre-
ceding the tone was designated as the "pre" period. The "during" period
commenced one second following the onset of the tone and lasted for
2 seconds, i.e., up to (not beyond) the onset of brain stimulation. Each
difference score represents a measure of the CR amplitude on a single
conditioning trial. The advantage of this method of determining CR
amplitude was that the duration of the CS was sufficiently long to permit
the CR to appear before brain stimulation on reinforced trials, so that it
was unnecessary to rely on test trials without reinforcement in observing
FIGURE 10. Photomicrographs from three of the series of cresyl-violet-stained

frozen sections from the brain of S 20. Middle photomicrograph shows actual loca-
tion of the electrode tip which is in the septal area to the right of the midline and at
the level of the rostral part of the anterior commissure. Plane of sectioning was
displaced from that of the electrode. Top photomicrograph shows section before
tip was reached, and bottom one shows intact section slightly posterior to the elec-
trode tip.
is
20 40 60 80 100 120 1 10 30 SO 70
ACQUISITION TRIALS EXTINCTION TRIALS
FIGURE 11. Acquisition and extinction curves for classically conditioned

heart rate slowing. N for acquisition was 20 Ss, for extinction 17 Ss.
Mean value for first extinction trial is plotted separately (see broken
line).
the progress of conditioning. Each point on the acquisition curve is a

mean based on 20 difference scores, while each point on the extinction
curve is based on ten difference scores. Acquisition is manifested by the
gradually increasing mean difference scores, while conversely, extinction
is manifested by the gradually decreasing mean difference scores. From
these results it appears, then, that with septal stimulation as US, the UR
of heart rate slowing was conditioned to a tone.
We should consider, however, whether these results could be explained
in terms of pseudoconditJoning (or sensitization). Sensitization usually
implies that the effect of the US is an activating or exciting one, which
is not the case in this experiment. As previously explained, septal stimu-
lation (in contrast with electric shock) appeared to have a quieting effect
on the animals. This in itself contraindicates a pseudoconditioning ex-
planation of the results. Moreover, the progressive increment in the CR
during conditioning and its decline during extinction argue strongly
against any non-learning explanation of the data. However, there is more
direct evidence against pseudoconditioning. While, as mentioned, it was
unnecessary to rely on test trials, the evidence from the first extinction
trial, a test trial (see Figures 8 and 11), was considered quite important
in ruling out pseudoconditioning. Figure 11 shows that on this test trial
the mean CR for the group was very nearly the same as the mean CR on
the last day of acquisition training. The CR on the first extinction trial
occurred 24 hours after the last brain stimulation and therefore could not
be explained as a reaction sensitized by recent brain stimulation. Nor
could the CR be explained as merely a sensitization reaction caused by
placing the animals in a compartment where brain stimulation had been
repeatedly given on previous days, because in a control condition it was
shown that, following six daily sessions of brain stimulation alone, tone
alone did not produce a significant mean heart rate response. The critical
dependence of the CR on pairing of CS and US seems therefore to have
been demonstrated in this experiment
Interpretation of the conditioning data in this experiment is complicated
by the fact that under operant conditions the US has rewarding proper-
ties. It is conceivable that if initial heart rate responses to tone at the
beginning of conditioning happened to be consistently in the direction
of slowing, the rewarding effect of brain stimulation could have reinforced
such a response. But analysis of data from the early part of conditioning
showed that this was not the case. On the first three trials the four best
conditioners all had two successive heart rate rises during tone (prior to
brain stimulation) and one animal (S 17) had three successive heart
rate rises. For the group as a whole on the first three trials, 51.85 per cent
of the trials were rises and 48.15 per cent were drops in heart rate during
tone (prior to brain stimulation). The argument might still be pressed,
however, that the effect principle is applicable later in conditioning when
by virtue of classical conditioning the balance of heart rate change with
tonal stimulation was tipped in the direction of slowing: that septal
stimulation, by means of its "rewarding" effect further strengthened the
CR (heart rate slowing to tone). To me this explanation seems im-
probable, though admittedly it can not be completely ruled out with
present data. To rule it out one would have to demonstrate heart rate
conditioning, using as US stimulation in an area of the brain other than
one eliciting ICSS (assuming that one of these areas is without autonomic
effects). There are some data, however, that seem strongly opposed to
the notion of operant conditioning of the heart rate slowing response. In
the first place, the rewarding effect of brain stimulation as gauged by
number of bar-presses was uncorrelated with ease of conditioning the
classical CR (heart rate slowing). For the group as a whole, the correla-
tion was only .03 between mean CR in the classical conditioning, and
mean number of bar-presses in the ICSS instrumental learning. Secondly,
it is interesting to note that S 8, one of the best classical conditioners,
actually failed to acquire the ICSS habit. Histology showed an electrode
placement very similar to that shown in Figure 10, a placement that in
other animals was associated with good acquisition; and I saw no signs
of aversive reaction to brain stimulation when I placed him on the bar.
But in the third acquisition session, when the mean bar-pressing rate for
the group was 9.59 presses per minute, S 8 didn't press the bar even
once, and during the last full acquisition session, when the mean bar-
pressing rate for the group was 11.02, S &s rate was only 0.2 (as com-
pared with 2.0 in his first acquisition session). S 8 had the lowest bar-
pressing rate of all the animals in the main group, but again, he was one
of the best classical conditioners. With septal stimulation so ineffective
in reinforcing bar-pressing in S 8, it seems most improbable that it was
effective as an operant reinforcer in the case of S 8's heart rate slowing
response to tone. Third, it is also interesting to note that S 15, the animal
with by far the highest bar-pressing rate, was one of the poorest classical
conditioners.
Earlier in this paper I dealt with the question of the heart rate CR as
an artifact of skeletal movements in anticipation of brain stimulation.
Here I would only stress the fact that there were no reliable reversals in
direction of CR and UR in this group of septal animals and that in the
best conditioners even the amplitude of the CR at the end of condition-
ing was remarkable in its approximation to that of the UR.8 In short,
these positive data considered together with the negative data for anticipa-
tory and skeletal artifacts encourage the idea that the conditioning
observed in this experiment was based on the formation of neural con-
nections, established according to the contiguity principle, in a manner
similar to that suggested by Hebb (1949) in his detailed description of
the cell assembly.
Before proceeding with the final discussion, a few additional remarks
concerning the available respiration findings may be made. Earlier in
this paper, evidence was presented to support the conclusion that the
slowing of heart rate, following septal stimulation, was not secondary
to a respiratory reaction. However, it may still be queried whether the
conditioned heart rate slowing may be secondary to a respiratory change
(e.g., a respiratory CR) even though the heart rate UR was not a
secondary reaction. But the available evidence seems to favour the con-
clusion that the heart rate CR was not dependent on a respiratory CR
or on any kind of respiratory reaction. Two of the best heart rate con-
ditioners failed to show reliable conditioning of respiratory rate; and
8
In some similar heart rate conditioning experiments with brain stimulation,
which he now has under way, Mr. Lloyd Gilden at McGill is obtaining further
supporting evidence for autonomic conditioning of this land, with CRs and URs in
the same direction.
In stressing the significance of similarities between CRs and URs in these experi-
ments, I do not intend to imply that such similarities are a sine qua non of all
conditioning. My intention is merely to state that these similarities strengthen the
case for conditioning in these particular experiments.
one of these subjects, though showing a highly reliable heart rate CR,
failed to show conditioning in either rate or amplitude of respiration.
In conclusion, careful examination of all the findings did not suggest
an alternative explanation that could account for the heart rate condition-
ing data as adequately as one based on the assumption that classical
conditioning had occurred (in the absence of reward that was contingent
upon the animal's response): that the UR was a heart rate slowing
reaction elicited by septal stimulation, and that the CR was also a heart
rate slowing reaction, its strength increasing progressively with continued
repetition of the CS-US pairings.
It may be noted that the term classical conditioning is appropriate
according to the original definition of Hilgard and Marquis (Kimble,
1961), that is, conditioning in which the CR is irrelevant to occurrence
of the US; and it may also be noted in passing that Pavlov's salivary
conditioning experiment did not conform to this definition of classical
conditioning. Hebb (1956) has put it this way:
. . . salivary secretion as studied by Pavlov is, by [this definition] not classical, but
instrumental. Not only must the dog reach for and seize the food, in Pavlov's pro-
cedure; he must also secrete saliva if the food is to be positively reinforcing. Dry
food in the mouth is noxious rather than rewarding and cannot be swallowed. Both
the primary reinforcement of food in the stomach and, to a great extent, the secondary
reinforcement of taste, are therefore contingent upon the specific response (salivation)
that is being conditioned (p. 165).
There is a closely related point. Contrary to conventional textbook

interpretations of Pavlov's experiments, it seems wrong to use them as
models for learning by contiguity. The response patterns appear too
complex to be completely accounted for by the principle of contiguity.
More direct evidence for the validity of the contiguity principle in con-
ditioning seems to be coming from the recent experiments involving
simpler associations like the conditioned arm-raising response to visual
cortex stimulation that Doty and Giurgea (1961) referred to as a
"functional absurdity."
Direct stimulation of the brain appears a promising technique in
conditioning studies, and it may be that certain motor areas in the brain
will be found to lend themselves more readily to conditioning of this
kind than will other areas. There seemed to be a hint of this in comparing
my heart rate conditioning experiment with experiments in which skeletal
movements were conditioned. For example, the very short intertrial
intervals that I used precluded conditioning in the Doty and Giurgea
(1961) experiments; and though I had no reversals of CR and UR in my
series, in two of the eight dogs conditioned in the Brogden and Gantt
9
(1942) study the CR and UR were dissimilar. The fact that my subjects
were rats while theirs were dogs must be kept in mind. But it could be
that the species difference is relatively unimportant and that conditions
such as the precise duration of the intertrial intervals do not make so
much difference in obtaining heart rate CRs as for obtaining skeletal
conditioning without reward. With further experimentation it may be
found that in general, autonomic responses condition more readily than
skeletal responses; but present evidence is, of course, insufficient to
support such a generalization.
Finally, it would, of course, be unwise to conclude too much from
the relatively few experiments with positive results. But the combined
findings, from the several experiments with evidence of learning in the
absence of reward, bear directly on problems that are of considerable
importance for learning theory. These combined findings support con-
tiguity-based learning concepts; and the important question of reinforce-
ment through contiguity (i.e., the question of learning in the absence of
reward) merits much further experimental investigation.
Progress toward the solution of an equally important problem, that of
the neurophysiological mediation of reward, may be accelerated by
further experiments with physiological recordings during intracranial
self-stimulation. At least this is the indication from initial findings which
are sufficiently positive to encourage further exploration of the ANS and
CNS changes correlated with reinforcing brain stimulations.
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ON CENTRAL AND AUTONOMIC NERVOUS SYSTEM

MECHANISMS IN CONDITIONING, LEARNING,

PSYCHOLOGY HAS COME A LONG WAY since physiological measures were

FIGURE 2. Drawing of subject in the free-roving

FIGURE 3. Diagram showing arrangement for recording respira-

FIGURE 4. Physiological tracings recorded during septal self-stimulation in S 17.

FIGURE 5. Physiological tracings recorded during septal self-stimulation in S 17

FIGURE 6. Drawing of subject in the restraining device

stimulation seemed helpful in getting the animals to lie quietly. This

EXTINCTION OF INTRACRANIAL SELF-STIMULATION

was extremely well controlled—almost machine-like. But, after the current

FIRST EXTINCTION TRIAL

FIGURE 8. Physiological tracings recorded during first extinction trial in classical

Problem of Neural Mediation of Reward

Conditioning of a Centrally Elicited ANS Response (in the Absence of

Integrated EEG 16 - 28 cps

FIGURE 9. Physiological tracings recorded during heart rate conditioning. Note

FIGURE 10. Photomicrographs from three of the series of cresyl-violet-stained

FIGURE 11. Acquisition and extinction curves for classically conditioned

the progress of conditioning. Each point on the acquisition curve is a

There is a closely related point. Contrary to conventional textbook

(First received August 29,1962)

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