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The Heart Rate Component of the Social Reflex

in Dogs: The Conditional Effects


of Petting and Person*
JAMES J. LXNCH ANI~ W. HoRsr~v.r CAN'I"r
The Pavlovian Laboratory, The lohns Hopkins University School of
Medicine, Baltimore, Maryland
Abstract--Five dogs were given a 480-cps tone followed by shock for
more than 200 trials. A 200-cps tone was then introduced followed by
a person petting the dog at the end of the conditional signal (CS) for
50 trials. Finally, the 480-cps tone-shock (T-S) sequence was reintro-
duced for five trials, after which the person entered the experimental
room and stood beside the dog during one additional T-S sequence.
It was observed that both the heart rate (HR) increase to shock, and
the HR decrease to petting could be conditioned rapidly (1-5 trials).
These findings are discussed in terms of the theory of stimulus substitu-
tion in classical HR conditioning.
After the person had been made part of a CS for petting, and the
T-S sequence reintroduced, the HR increase during the CS was reduced.
The HR response to the shock, however, was greater than the response to
this US when the dog was alone. A control group, given the same T-S
sequence with a person present who had not been a CS for petting, did
not show any significant HR changes from the usual response given to
the T-S sequence.
It is emphasized that these findings, in conjunction with earlier re-
ports, indicate that the cardiovascular system may be a valuable index
in studying the psyehophysiology of socialization processes.

Wrm~E s~n~_~rc conditional reflexes in the dog, Pavlov n o t e d


that the experimenter h a d a m a r k e d inhibitory effect on salivary
conditional reflexes. At first h e considered the person one of a
n u m b e r of excitatory stimuli, but later investigations of specific
responses to specific people led him to postulate the existence of a
"social reflex" in the dog. He discussed this reflex w h e n he wrote:
"Finafly, we have come across in our dogs a definite social reflex,
operative u n d e r the influence of an agent of the social surroundings.
Dogs and their wild ancestors, wolves, are h e r d animals, and man,
owing to their ancient, historical association together, represents
for t h e m a 'Socius" (Pavlov, 1928, p. 368)."
A n u m b e r of recent studies have elaborated various aspects of
the social reflex in the dog. For instance, m a r k e d behavioral effects

* This research was supported by Grant HE 06945 from the National


Institutes of Health, and was conducted at the Pavlovian Laboratory, Veterans
Administration Hospital, Perry Point, Maryland. Special thanks are due to
Gene Isom for his technical assistance, and to Shoji Kakigi for his suggestions
in the writing of this manuscript.
69
Conditional Reflex
~'./ L Y N C H A N D GANTT Apr.-June, 1968

of early social isolation have been observed in dogs (Hebb, 1955;


Fisher, 1955; Fuller, 1963; Melzack and Scott, 1957; Thompson and
Heron, 1954). Stanley (1965) and Stanley, et al. (1966) have
shown that the passive presence of a person (a person present but
not touching the dog) increased the running speed of a dog. Gantt,
et al. (1966) and Lynch and McCarthy (1967) have observed that
petting reduced the usual amount of spontaneous and conditional
motor activity, while McIntire and Colley (1967) have noted that
petting can be used as an effective reinforcement in shaping and
maintaining performance in dogs.
Along with the behavioral observations of the social reflex in
dogs, recent studies have indicated that this reflex also is reflected in
physiologic responding, particularly in the cardiovascular system.
Gantt, et al. (1966) have observed that when a person enters an
experimental room in which a dog has been isolated, the person's
entry as a rule elicits a marked tachycardia in the dog. If the person
pets the dog, however, there is generally an abrupt and marked
bradycardia.
Some factors that influence the HR response to a person have
been investigated. Royer and Gantt (1961) observed that the HR
response of the dog to a person entering an experimental room
varied for different people. Later research revealed that the HR
response of the dog to a person was contingent on the type of rein-
forcement associated with that person (Lynch and McCarthy, in
press). Although during the previously cited stimulus conditions
the presence of a person did have marked effects on the HR of a
dog, it has also been reported that the passive presence of a person
during a tone-shock sequence has little lasting effect on the HR-CR
(Lynch and McCarthy, 1967). Since the effect of a person does de-
pend on the type of reinforcement associated with that person, the
question is raised whether the Effect of Person during a tone-shock
sequence might also depend on what reinforcement had been asso-
ciated with the person previously? That is, if the person were first
made part of a CS for petting, would he then affect HR response
during a tone--shock sequence differently than if he had not been
made part of a CS for petting?
The HR-UR response to petting also has been investigated sys-
tematically. Anderson and Gantt (1966) demonstrated that petting
during shock that was not preceded by any warning signal sig-
nificantly reduced the usual tachycardia that accompanied the shock.
Subsequently, it was noted that petting during a CS and during the
shock US eliminated both the conditional and the unconditional
tachycardia which normally occurs, and in a significant number of
Volume 3
Number 2 T H E H E A R T RATE C O M P O N E N T 71

trials changed the HR-CR and the HR-UR to a bradycardia (Lynch


and McCarthy, 1967). These studies support the thesis that petting
is an unconditional stimulus for the dog, or at least elicits a HR
response that is learned at some early critical period of socialization.
An initial test of whether petting is an US was made by Gantt,
et al. (1966) in a dog in which they paired a CS with petting. They
noted that the bradycardia response to the petting could be con-
ditioned. When Lynch and McCarthy (in press) paired a person's
entry into an experimental room with petting, the HR response of
the dog to the person's entry was significantly different from the
typical HR response elicited by a person's entry when paired with
other reinforcements. However, the HR response to a person fol-
lowed by petting was a tachycardia. In light of the initial work of
Gantt, et al. (1966), and the subsequent evidence supporting the
hypothesis that petting is an US, the question is raised whether a
CS followed by petting will elicit a conditional bradycardia during
the CS consistently?
Method
Subjects
The Ss were 10 adult, male, mongrel dogs; five control and
five experimental dogs.
Apparatus
The apparatus used in this experiment has been described pre-
viously (Lynch, 1967). Basically, it consisted of a soundproof
chamber in which the animal was isolated, programming equipment,
and a four-channel Offner Dynograph for the recording of physio-
logic responses.
Procedure
The procedure used in this study consisted of five phases; habitu-
ation training, orienting, tone-shock (T-S) conditioning, tone-pet-
ting (T-P) conditioning, and finally, the interactive influence of a
person on aversive conditioning. The habituation and orienting pro-
cedures have been described elsewhere (Lynch, 1967) and were
designed to accustom the animal to the experimental chamber, ex-
tinguish the HR--orienting reflex and the motor orienting reflex to
the tones, etc.
During conditioning, a 480-cps tone, 79 db, was presented.
Twenty trials were given daily, with variable intertrial intervals
averaging two minutes. The CS-US interval was 41 sec., with the
US occurring during the last 1 sec. of the CS. The US was an
unavoidable shock of suflqcient intensity to elicit full unconditional
Conditional Reflex
72 L Y N C H AND G A N TT Apr.-~une, 1968

leg flexion (3--6 ma. ). Twenty trials of T-S were given per day and
all dogs were given more than 200 trials in order to insure con-
stant conditional leg flexion and a stable HR-CR and HR-UR. Stable
HR-CR's and UR's were evaluated by noting a marked reduction
in trial-to-trial response variability (see Lynch, 1968).
Following this T-S conditioning, each of the five experimental
dogs was presented with a 200-cps tone, 11 see. in duration, fol-
lowed by ten seconds of petting. Ten trials of this T-P condition
were given daily, for five experimental sessions. The petting was
initiated during the last second of the CS. The intertrial intervals
between tones were randomized, averaging out to two minutes.
During the intertrial interval, the person stood quietly in the ex-
perimental room. The same person was used throughout (standing
and petting) with all the dogs.
After Trial 50 of T-P, the person left the experimental room, and
the 480-cps T-S (11 see. in duration) was reintroduced for five
trials. After the fifth trial, the person re-entered the experimental
room and stood quietly beside the dog for three minutes. The 480-
cps T-S was then presented, the person standing quietly (without
touching the dog) during the entire period.
The five dogs in the control group were given 11 sec. T-S con-
ditioning for more than 200 trials, and then presented five additional
trials at the beginning of an experimental session. After this, a
person who had not been a systematic signal for any reinforcement
entered the room and stood beside the dog while the 480-cps T-S
sequence was run for an additional trial. This control was necessary
to ascertain whether the person was merely acting to produce ex-
terual inhibition on HR during the CS and US. The sequence of
experimental conditions presented to both the control and experi-
mental groups, then, was as follows.
Experimental Group Control Group
1. Tone-shock conditioning for 1. Tone-shock conditioning for
more than 200 trials more than 200 trials
2. Tone-petting for 50 trials 2. m

3. Tone-shock for 5 trials 3. Tone-shock for 5 trials


4. Tone-shock with person pres- 4. Tone-shock with person pres-
ent for 1 trial ent for 1 trial

Measurements
The HR response to the CS and to the US was established by
counting the number of R-waves in consecutive 10-see. intervals,
viz., before the onset of the CS, 10 see. during the CS, and 10
see. after the US for each of the trials. The total number of R-waves
p-?r
Volume 3 THE HEART RATE COMPONENT IO
Number 2

during each of these three conditions was then summated for all
the trials in a given day and the results converted into beats per
minute.

Results
The results of this study indicate that both the bradycardia
elicited by petting and the tachyeardia elicited by electric shock
are rapidly conditioned to stimuli paired with these reinforeements
(1--5 trials). Figure 1 illustrates that not only the direction of con-

180

0--0 200 cps tone & petting Shock with


I# 9 480 cps tone & shock Person Present
170 0---- 9 480 cps tone & shock but
with a person present 9
/
/
/
160 / Shock
/
480 cps tone

m 150 - 9 - ~ //
/
/
140 /
/
/
/
Z
o / 480 eps tone with
130 & Person Present

120 s

II0
O ~ 200 cps, tone
Do~ "s Pe,tted
O ~
I00 ~ 0

o .,, I I ., , I
10 s e c S . I0 secs. 10 secs.
Pre CS During CS After US

FIc. 1. Heart rate response in five dogs to condigonal signa~ for petting
and shock and signal for shock with a person present.
Conditional Reflex
74 L Y N C H AND GANTT Apr.-June, 1968

TABLE I. Heart Rate Responses; Person Present and Person Absent

Five Trials T-S


Mean Heart Rate T-S -~- Person Present
Pre CS During CS Post US Pre CS During CS Post US

Control
Dogs
A 114" 22.2* 19.8 126 20 23
B 86.4 18.4 22 120 22 24
C 114 25.8 22.2 102 19 19
D 91.2 20.8 17.8 108 23 17
E 96 20.8 20.6 84 18 18
MEa_~ 100.3 21.6 20.6 108 20.4 20.2
Experimental
Dogs
A 141.6 36.0 33.6 126 0 66
B 159.0 6.6 41.4 162 18 72
C 114.0 34.8 31.8 114 30 18
D 104.4 8.4 18.0 102 0 48
E 100.8 28.8 31.2 90 6 48
MEAN 123.9 22.9 31.2 118.8 10.8 50.4

* Pre-CS HR is the mean HR (beats per min.) for that condition. The
during-CS and post-US heart rates are the HR differences between the Pre-CS
HR and the HR during the CS or US. Thus ff the pre-CS HR was 114 and the
during-CS HR 136.2 beats per minute, the difference score of 22.2 is given.
All HR differences during the CS or post-US periods represent increase or no
change from pre-CS HR levels.

ditional H R change, but also the degree of that change is related


to the unconditional H R changes.
T h e conditional bradycardia during the T - P is significantly dif-
ferent (p < 0.01) from the pre-CS HR, and the unconditional H R
response to petting is also significantly different from t h e pre-CS
H R (p < 0.05). The conditional and unconditional H R changes
during the T - P are not significantly different from each other.
T h e conditional and unconditional changes to the T-S are both
significantly different from the pre-CS H R ( p r e - C S - d u r i n g ,
p < 0.05; p r e - C S - p o s t US, p < 0.01), but not significantly different
from each other.
In addition, this figure shows the effect that a person ( w h o
h a d previously b e e n part of a CS for petting* ), present during a
T-S sequence, h a d on the conditional and unconditional H R re-
sponse. I n particular, it can be seen that a person present during
a T-S sequence reduces the usual tachycardia to the CS (p < 0.20)

* It is recognized that the role of person is a complex one: his appearance


may be a CS, while other actions, for example, petting, may be complex US's.
Volume
Number 32 THE HEART RATE COI%[PONENT "/5

but increases the HR response to the shock itself (p < 0.10). The
difference between the during-CS and the post-US HR with the
person present is significant (p < 0.05).
A comparison of the HR differences to the T-S sequence with a
person present in both the control and experimental groups is seen
in Figure 2 and Table 1. T tests of the difference scores in the con-
trol group reveal that the HR is not significantly different during the
CS or shock US whether the person is present or the dog is alone,
although in both conditions the heart rates are significantly different
from pre-CS levels. (In all cases, p < 0.05). The conditional HR-
CR with the person present, however, is lower, although this change
is not significant. T test comparisons of the HR difference scores
from the pre-CS to the during-CS, in both the control and the
170
0 Shock
I
Tone with a Person present /
Q ~ O who had not previously been /
160 a CS for Petting i
/
Tone with a Person present /
O-- --O who had previously been a CS /
for Petting /
150 I
/
/
/
140 !
/
/
/
130 I
ao
0
s j
s S
s
4"*' 0
120 0 Shock

~ 110
0

I00

0
I0 secs. I0 secs. i0 s e c s .
Before CS During CS After US

FIG. 2. The varying effects of person on the conditional and unconditional


heart rate response to shock.
76 LYNCH AND GANTT Conditional Reflex
Apr.-June, 1968

Fxc. 3. The Effect of Person on an aversive conditional signal.

experimental groups, indicate that when the dog was alone the
two groups were not significantly different in the degrees of the
conditional responding. However, significant differences were ob-
served between the control and the experimental groups in the
HR difference scores during the CS and post-US periods when the
person was present (p < 0.001).
In the experimental group, the pre-CS HR was significantly
lower during petting conditioning than during shock conditioning
(p < 0.05).
Finally, in Figure 3, an example of the actual HR and respiratory
tracings for one of the dogs during each of the three experimental
conditions is shown.
Volume 3
Number 2 T H E H E A R T PLATE C O M P O N E N T 77

Discussion of Results
The present study indicates that the passive presence of a
person who previously had been associated with petting can reduce
the conditional tachycardia which usually occurs during aversive
shock conditioning, while at the same time it significantly increases
the HR response to the shock itself. This study further delineates
the effects that a person has on HR responding during aversive con-
ditioning, and indicates that the effect of a person is highly con-
tingent upon prior stimuli associated with that person (Lynch and
McCarthy, in press). The previous observation that petting is an
effective reinforcer to the dog which can be used as an unconditional
stimulus is also supported (Anderson and Gantt, 1966; Gantt, et al.
1966; Lynch and McCarthy, 1967 and in press).
In the previous studies (Anderson and Gantt, 1966; Lynch and
McCarthy, 1967 and in press) it had been shown that petting
during an aversive situation could reduce or even reverse the direc-
tion of HR conditional and unconditional responding. The present
study extends these findings to include the observation that a per-
son can also reduce the HR-CR to an aversive CS, ff that person
previously has been associated with petting the dog. Somewhat
paradoxical is the observation that the HR-UR to the shock is in-
creased when this same person is present. Behavioral observations
of these experimental dogs indicated that they did not appear to
"expect" to be shocked; during the aversive CS they simply looked
at the person and failed to give their usual conditional foot flexion.
The control dogs all continued to give conditional foot flexion during
the aversive CS with a person present.
A further delineation of the conditional and unconditional effects
of a person and petting on the autonomic responding of dogs is
critical in the light of the recent observation of Murphee, et al.
(1967) that the HR response of a dog to a person is markedly
different in normal and neurotic dogs.
Although the durations of the CS were different for the control
and experimental groups during the initial T-S training, no sig-
nificant differences in conditional HR responding were observed
between these groups when the same CS durations were used.
Three major theoretical mechanisms have been proposed to
account for the type of CR observed in classical HR conditioning:
drive reduction, mediation, and stimulus substitution (Zeaman and
Smith, 1965; McDonald, et al. 1963; Notterman, et al. 1952). Zeaman
and Smith (1965, p. 378) define these three theories as follows:
Classical stimulus substitution theory holds that the temporal pairing of
CS and US permits CS to be substituted for US in its control of UR. It
78 LYNCH AND GANTT Conditional Reflex
Apr.-June, 1968

would be expected, according to this view, that UR and CR would be


similar in form. Mediation theory maintains that the temporal pairing of
CS and US results in the association of CS with a mediating state of re-
sponse, which in turn affects some aspect of response, not necessarily UR.
Examples of mediating states are anxiety and expectancy; examples of
mediating responses in cardiac conditioning include responses of the
respiratory or skeletal musculature. According to this view the CR and
UR need not have similar topographies. Drive reduction theory states
that the particular aspect of responses occurring at the time of drive
reduction becomes associated with CS. This theory predicts that the
similarity in form of CR and UR is under the control of manipulable,
experimental conditions.
Zeaman and Smith (1965) suggest that a critical test of stimulus
substitution could be made if a noxious US could be found that
elicts a decelerative HR-UR. Although the present study did not
have a noxious US that elicited a decelerative HR-UR, nevertheless
the two stimuli used did elicit opposite HR unconditional responses
within the same animal. In this respect the data from our study
support the theory of stimulus substitution in classical conditioning,
since both the degree and the direction of the HR conditional re-
sponding to the CS's for petting and shock were similar in direction
and degree to the H R - U R elicited by their respective US's.
The fact that the pre-CS was considerably lower during petting
conditioning than during shock conditioning indicates that HR ade-
quately reflects generalized conditional changes in the environment.
That is, if the situation is more aversive, the resting HR is higher
than ff the conditioning situation is less aversive. An example of
the interaction of these two factors is seen in Figure 1, where the
animal is in aversive shock conditioning but with a person present
who previously has been part of a CS for petting. In this case, the
pre-CS HR falls in between the pre-CS HR's for the petting and
shock conditions.
The fact that the HR to US is higher after it is inhibited by the
presence of Person would be attributed by some Pavlovians to posi-
live induction (Fig. 1). This law states that a positive stimulus is
stronger when it is applied after a negative stimulus than if it is
applied after another positive stimulus. Induction played a major
role in many of Pavlov's explanations. Although this phenomenon
of induction is often seen, one difficulty among others is to determine
the time relations necessary to know when induction occurs and
when irradiation occurs. These difficulties were recognized by
Pavlov. He said (1923) :
For the present all remains in darkness-the spread of the inhibitory proc-
ess, as well as the phenomenon of the elaborated reciprocal induction,
and many other of the above mentioned phenomena, above all the fact
of the transformation of a positive excitation into the opposite negative
process, and vice versa.
Volume 3
Number 2
THE HEART RATE COMPON-ENT 79

In 1927 Pavlov had extended the time limits of induction:


The duration of induction varies from several seconds to one or two
minutes. The cause of this variation has not yet been stdBciently investi-
gated. (Anrep, page 191)
And in 1932 the time was made even less definite.
Positive induction is known with both unconditioned and conditioned
reflexes, appears either immediately or for some time after the inhibition.
(Pavlov, Vol. II, page 104)
Notwithstanding the lack of clarity in regard to induction, one
should take every opportunity to note the occurrences that seem to
fall into this pattern. There is evidently a short-term induction that
is seen for very short periods, v iz., fractions of a minute, and a long-
term induction that occurs over periods of hours, days, or months.
The mechanisms are probably entirely different. An example of the
latter is the stage of increased activity after a long confinement,
either in seclusion or from illness.
This long-term induction obviously cannot be the same phenom-
enon as the immediate induction. Probably it is more properly
referable to the process of autokinesis, of reactivity among stronger
depots of forces in the nervous system. These long-term, chronio
states are much more difficult to study and identify. They are the
interesting prospects for the future investigator.
Finally, this study is an example of the growing evidence that
there are psyehophysiologie concomitants of social interactions and
that the cardiovascular system in particular reflects these processes
in the dog. These internal response systems complement the already-
well-documented evidence of behavioral indexes of social respond-
ing (Scott, 1945, 1950, 1956).
A major question emerging from this research is whether com-
parable physiologic reflexes exist in man; if so, what response sys-
tems would describe these processes adequately? Previous research
had indicated that psychophysiologic changes can be elicited from
the human being during social interactions. The problem raised by
the present research is to attempt to analyze whether there is a
specific social-psychophysiologicunconditional reflex system in man
which can motivate behavior.

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