Introduction : When adult male Old
World monkeys yawn, lip retraction, the opening
wide of the mouth, and the climactic tilting of
the head upwards and backwards combine to expose
the teeth clearly and to enhance the visual
impact of the canines. Yawning is performed more
frequently by adult males than by other age-sex
classes, and its rate of occurrence is
influenced by serum testosterone levels.
Observations of increased rates of yawning in
situations of tension or social conflict have
given rise to the interpretation of yawning as a
visual signal communicating an adult male's
potential for aggressive intervention, with
whether the yawn is directed toward an opponent
being an important distinction
Given the apparent communicatory role of
yawning in adult male Old World monkeys, the
question arises as to whether yawns can be
produced voluntarily. The widespread distinction
between directed and nondirected yawns implies
that the orientation of the act, at least, is
controllable. Some data from observational
studies may also be taken as indirect, albeit
weak evidence for such control. For example, in
olive baboons, the frequency of nondirected
yawning in the proximity of other newly
transferred males was positively correlated with
the condition of the displaying male's canines.
In Celebes macaques, rates of vawning by adult
males varied with changes in their
dominance status. There is,
however, little direct evidence. In the only
previous experimental study on whether nonhuman
primates can control their rate of yawning,
Louboungou and
Anderson obtained increased rates in two
adult male pigtailed macaques through the use of
food rewards. Extinction and recovery of yawning
occurred when rewards were withdrawn and
reinstated, respectively. These findings were
striking and unexpected. In the present study we
used adult males of another species of macaque,
Macaca tonheana, to examine further the
possibility of learned control over yawning, a
behavior that Barbizet
has described as "halfway between a reflex and
an expressive movement."
Materials and methods :Subjects and
Housing : The subjects were two group-reared,
adult male tonkean macaques, Macaca tonkeana,
recently removed from their group and living in
individual indoor-outdoor cages. The subjects
("Nemo," 10.6 years old, and "Chou," 6.10 years
old) were in visual contact with each other, but
they interacted very little, either during
experimental sessions or at other times. They
were also in contact with their former group
except during testing. Food (commercial monkey
pellets) and water were available ad
libitum.
Procedure : For all experimental sessions,
each lasting 1 hour, the subjects were confined
to the indoor part of their cages (1.9 X 1.4 x
2.0 m for Nemo, 2.9 x 1.4 x 2.0 m for Chou). The
two experimenters each worked with one subject
for all 22 sessions, which were conducted in ten
phases over a 25-day period as follows: 1)
Baseline (N = 2): spontaneous yawns were
recorded; 2) Free rewards (N = 2): 20 small
pieces of dried fig or fresh banana were given,
distributed randomly throughout the session and
independently of the subject's behavior; 3)
Continuous reinforcement (CR) (N=4): All yawns
produced by the subject were immediately
reinforced by the experimenter, who gave the
reward (a piece of dried fig or fresh banana) by
hand; 4) Extinction EXT (N = 2): No rewards were
given; 5) CR (N = 2); 6) EXT (N = 2); 7) CR (N =
2); 8) EXT (N =2); 9) Fixed ratio 3 (FR-3)(N =
2): a reward was given only after the subject
produced three yawns; 10) EXT (N = 2). The
subjects were always tested simultaneously.
Results : Figure 2 shows the results
for each subject. To simplify presentation of
the data, phases 1 and 2 have been combined to
give BASE sessions, the CR phases 3, 5, and 7
have been combined, and EXT phases 4, 6, and 8
have been combined to give EXT 1. The data
points in Figure 1 represent the average number
of yawns produced in the four 15-minute blocks
of each session.
During baseline sessions the subjects
typically yawned between 2 and 4 times per
15-minute block, although Nemo yawned more
frequently at the start of these sessions,
apparently in response to being confined to the
indoor cage section. Continuous reinforcement of
yawning increased overall rates o the behavior
in both subjects. This was especially evident in
the first 15-minute block, with performance
tapering off later in the session as the
stibjects became satiated. However, in both
subjects yawning rate in the last 15-minute
block of CR sessions remained higher than in the
corresponding block of baseline sessions.
The first 15-minute block of extinction
sessions was marked by frequent yawning in both
subjects. With the continued absence of
reinforcement during extinction sessions there
was an eventual return to baseline levels of
yawning.
The most striking trends emerged during the
FR-3 sessions. Chou averaged a peak of 16 yawns
during the first 15-minute block in this
condition. His yawning rate dropped to around 5
in the following two blocks (presumably because
of satiation), then rose again during the final
block. Nemo produced 15.5 and 17 yawns in the
first two blocks respectively, 3.5 in the third
block, and 6 in the final block.
In the final two extinction sessions, both
subjects showed higher rates of yawning at the
start of the session than at the end of FR-3
sessions. Both subjects then produced their
lowest averages for any 15-minute block during
these extinction sessions, although there was an
unexplained increase (to 8.5 yawns) in the final
block by Chou. There were no obvious behavioral
signs of frustration (e.g., cage-shaking,
scratching) during extinction.
Discussion : This study has shown that
adult male Macaca tonkeana can control their
yawning behavior to the extent that they will
produce yawns to obtain food-rewards, and reduce
their rate of yawning when food is no longer
contingent upon the behavior. These results
confirm the possibility of volitional control
over yawning reported by Louboungou
and Anderson for Macaca nemestrina However,
whereas in that study the conditioned act in one
subject was shaped through successive
approximation, in the present study both
subjects were rewarded from the start only for
naturally occurring yawns. It is also noteworthy
that the present positive results were obtained
using
-1) prized tidbits as reinforcers, without
food deprivation;
-2) relatively spacious caging conditions in
which the subjects could move around and
distance themselves from the experimenters. It
seems likely that more traditional operant
procedures including spatial restraint and food
restriction would lead to even more clear-cut
evidence for yawning as a conditionable
response.
Steklis and Raleigh describe the important
role of operant conditioning studies of
communicative acts in the comparative approach
to the neurobiology of communication in
primates. Such research bas given convincing
evidence for voluntary production of
vocalizations in a range of primate species
freviewed by Pierce, but there is no
corresponding evidence regarding the production
of facial expressions. Steklis and Raleigh point
out that the low spontaneous rate of facial
expressions presents a problem for operant
paradigins, and Louboungou and Anderson felt
that socially eliciting the to-be-reinforced
facial expression created an emotional state in
the subjects that interfered with learning.
Satisfactory experimental paradigms for operant
conditioning studies of primate facial
expressions remain to be established, but in the
meantime the positive results for yawning
suggest that the attempt is worthwhile.
One aspect that was not covered in detail in
the present study concerns the motoric
components of the yawns produced. One subject
(Chou) often seemed to struggle, mouth slightly
open and rounded, to produce yawns, and
sometimes abandoned the attempt. The other
subject produced a mixture of "slow" and "fast"
yawns, the latter resembling yawns produced when
the subject was released into the outdoor cage
section where he regained visual contact with
his former group. Several authors have
distinguished between yawns that occur in
fatigue and those more readily identifiable as
displays, positing differences in the extent of
teeth-exposure, earflattening, and
eyebrow-raising. A finer analysis of the
components of yawns, possibly using videotape,
could help clarify such differences, as well as
the degree of conditionability of the two types.
In any case, if some yawns funetion as a visual
display, it would be useful for an individual to
be able to control their production according to
the situation. This ability has been
demonstrated in the present study.
Conclusions
Individually housed, adult male Macaca
tonkeana learned to produce yawns for food
rewards and eventually reduced their rates of
yawning when rewards were no longer available
(extinction).
Adult male macaques therefore appear to be
able to control yawning.
It remains to be determined to what extent
"true" and "display" yawns are distinguishable,
and whether they are equally conditionable
Anderson JR;
Wunderlich D Food-reinforced yawning in
Macaca tonkeana American Journal of Primatology
1988; 16; 165-169
-Anderson
JR et al Contagious yawning in chimpanzees
The Royal Society Biology Letters may 2004
« It is
ironic that testosterone "the male sex hormone,"
is more closely associated with the yawning rate
than with the mounting or intromitting rates
» Charles Phoenix
Sexual
steroids
exert several effects on both central
dopaminergic and oxytocinergic systems by acting
either at the genomic or membrane level
