-
-
- Contagious yawning and laughter in humans
offer insights into a variety of problems in the
neural, behavioral, and social sciences.
Contagion is the probable response of "stimulus
feature detectors" triggered specifically by
yawns in the visual domain and laughs in the
auditory domain (Provine, 1986, 1989b, 1992,
1996a). It does not require conscious effort for
an observer to imitate a yawning or laughing
person. In the language of classical ethology,
these neurological stimulus detectors would be
"innate releasing mechanisms" (IRMs) evolved to
detect the "releasing stimuli" of yawns or
laughs (Alcock, 1989; Provine, 1986, 1996a).
Such stimulus feature detectors are more likely
to have evolved to select the simple,
stereotyped, species-typical acts of yawning or
laughing than more arbitrary and variable
behaviors learned during a lifetime of the
individual. Because observed yawns or laughs
trigger their respective neurological detectors
to evoke identical acts, contagious yawning or
laughter may be used to assay the activity and
determine the selectivity of the underlying
detection process. Contagious behavior, thus,
provides a novel, noninvasive approach to the
neural basis of sensory feature detection.
-
- The study of species-typical and stereotyped
yawning (Provine, 1989b) offers advantages over
other approaches to the detection of faces (a
visual feature) that rely on neuropsychological
studies of rare clinical conditions (i.e.,
prosopagnosia) (Meadows, 1974; Whiteley &
Warrington, 1977) or the electrophysiological
recording of face-specific brain neurons in
animal models (Bruce, Desimone, & Gross,
1981; Kendrick & Baldwin, 1987; Perrett,
Mistlin, & Chitty, 1987; Perrett, Rolls,
& Caan, 1982). In the auditory domain, the
search for a detector for structurally simple,
stereotypic, and species-typical laughter offers
advantages over more complex and culturally
varied speech (Provine, 1992, l993a, l996a). The
simplicity, stereotypy, and species typicality
of yawning and laughter offer similar tactical
advantages in the search for motor pattern
generating circuits (Provine, 1986, 1996a;
Provine & Yong, 1991).
-
- In studying contagious yawning and laughter,
we move seamlessly from the neural to the social
level of analysis. Yawning and laughter offer a
rare opportunity to examine the neurological
basis of that significant but neglected class of
social behavior-contagion (Provine, 1989b;
Provine, 1992). Typically, social psychologists
focus on behavior learned during the life time
of individuals and neglect innate or
neurologically mediated social behavior. Social
psychologists describe contagious-like behavior
in the context of higher level processes such as
"social facilitation," "conformity," "peer
pressure," or "modeling," and seldom consider
the possible biological roots of contagious
phenomena.
-
- Because the biologic and genetic
determinants of yawning and laughter are
stronger than that of many behaviors studied by
social scientists, they should not be relegated
to the category of "interesting footnotes." We
should not segregate them from other, more
familiar, social acts shaped more directly by
learning and experience. A thoughtful position
on such matters is offered by an expert on
behavioral contingencies, B. F. Skinner (1984).
When asked to respond to the challenges to
operant behavior by the discovery of "biological
constraints on learning," "feature detectors" in
sensory systems, and "pattern generating
circuits" in motor systems (Provine, 1984a),
central themes of this chapter, Skinner (1984)
replied "that a given species is predisposed by
its genetic history to see particular stimuli in
preference to others or to behave in particular
ways in preference to others are facts of the
same sort. A different kind of selection has
been at work." In other words, the contingencies
of natural selection can shape structure and
behavior during phylogenesis in a way similar to
the process that shapes behavior, during the
life of the individual.
-
- Contagious yawning and laughter provide
insights into imitation, a common topic in this
book, and a process of general behavioral
significance (Piaget, 1951; Provine, 1989a).
Instead of venturing into the semantic
quicksands of definition, this chapter has the
more modest goal of broadening the range of acts
evaluated in imitation studies. Consider, for
example, the controversy over the existence and
nature of facial imitation by human neonates
(Meltzoff & Moore, 1977, 1983). Most
researchers of facial imitation suggest the
involvement of high-level cognitive processes,
and have not considered the precedents of
contagious yawning and laughter. Although
contagious behavior may not qualify as imitation
as commonly defined, it is a ubiquitous, ancient
form of social coupling that coexists with
modern, consciously controlled social behavior
(Provine, 1986, l989a, b, 1992).
-
- This chapter describes contagious yawning
and laughter and shows how these acts can be
used to study a variety of issues in the neural,
behavioral, and social sciences. The
neuroethological approach taken here has a
strong descriptive foundation. Consequently,
this account begins with the description of the
motor acts of yawning and laughter because, in
the case of contagious behavior, the motor act
is both the stimulus and the response, and
defines the nature of the stimulus feature
detector supporting contagion.
-
-
- YAWNING
-
- Yawns as Stereotyped Action Patterns
-
- The word for yawning is derived from the Old
English "ganien," meaning to open wide as in
gape. Yawns are slow, involuntary, gaping
movements of the mouth that begin with a slow
inspiration of breath and end with a briefer
expiration. Yawning is a behavior of the type
called "fixed," "modal," or "stereotyped," by
ethologists (Alcock, 1989; Provine, 1986). The
term "stereotyped action pattern" will be used
here to refer to such acts. Consideration of
yawning will begin with a description of its
duration, frequency, and intrasubject stability.
These descriptions define yawning and provide
baseline data necessary for later
experiments.
-
- The mean yawn duration was 5.9 ± 1.9 s
(SD) for the 34 of 37 subjects who yawned at
least once during the observation period (2. The
formidable problem of getting subjects to yawn
in the laboratory was solved by having them
'think about yawning" and record their own yawns
by pushing a button at the start of a yawn and
keeping it depressed until the yawn is complete.
This technique avoids inhibitions associated
with the well-known social sanctions against
public yawning. Unless otherwise noted, this
procedure was used to induce and record yawns.)
(Provine, 1986). The mean duration of yawns for
individual subjects ranged from 3.5 to 11.2 s.
Yawning frequency of the 34 yawning subjects
ranged from 1 to 76 (X = 27.5 ± 18.4)
during the 30-min period of observation, an
average rate of about one yawn per min. The
periodicity of yawns, the onset-to-onset
interyawn interval, for the 31 subjects
performing at least two yawns, was 68.3 ±
33.7 s. No significant correlation was detected
between yawn duration and interyawn interval,
indicating that infrequent yawners did not
compensate by performing long yawns and vice
versa. (The significance of this finding for
respiratory function is considered below.)
Whatever their style, individual yawning
patterns were stable. The frequency and duration
of yawns performed by the same subjects during
10 min sessions separated by 1 to 3 weeks were
correlated significantly.
-
- Once a yawn is initiated, it goes to
completion with the inevitability of a sneeze.
Yawns are hard to stifle. The implications of
this experience were examined by having subjects
yawn with clenched teeth. This procedure tests
for the effects of eliminating or modifying
movement-produced feedback associated with the
gaping component of the yawn while permitting
normal respiration through the clenched teeth
(Provine, 1986). The frequency and duration of
normal and clenched-teeth yawns as estimated by
the respiratory component were similar. Thus,
the underlying motor pattern generator for
yawning was able to run normally with abnormal
sensory feedback. However, subjects reported
that such yawns were unpleasant, did not satisfy
the urge to yawn, and gave the impression of
being "stuck" in midyawn. The gaping of the jaws
must be performed to achieve a satisfying yawn;
the respiratory component is insufficient. Try a
clenched-teeth yawn yourself.
-
- Another yawn variant is informative. Try a
"nose yawn" in which your lips remain sealed and
you inspire through the nose. Most subjects
report being unable to perform nose yawns
(Provine, Tate, & Geldmacher, 1987). Unlike
normal breathing that can be done with equal
facility through either the nose or mouth, yawns
require inhalation through the mouth. The
difficulties of performing the nose and
clenched-teeth yawns suggest that the principal
function of a yawn is not respiratory; deep
breaths can be taken through either the clenched
teeth in the clenchedteeth yawn, or the nose in
the nose yawn.
-
- The function of yawning is elusive. However,
one of the most common popular explanations of
yawning can be rejected. Yawning is not a
response to elevated CO2 or decreased 02 in the
blood or brain. Yawning by laboratory subjects
was neither increased by breathing a gas mixture
high in CO2 (3% or 5%), nor inhibited by
breathing 100% °2 (Provine et al., 1987).
(The normal composition of air is 20.95% 02,
79.02% N2 and inert gases, and .03% CO2.)
However, both the CO2 and the 02 conditions
increased breathing rate, providing clear
evidence that they had evidence suggest that the
yawn should be considered a form of stretch and
that investigations of yawn function should
include the correlates of stretching. (Yawning
may have evolved as the facial component ofa
generalized stretched response that has an added
respiratory element (Provine, Hamernik, &
Curchack, 1987). However, given the phylogenetic
antiquity of yawning, it is also possible that
stretching evolved after and may be an
elaboration and caudal extension of a yawn, the
primal stretch).
-
- Although not studied systematically, there
are several significant differences between
yawning and stretching. There is less conscious
control over yawning than stretching, yawning is
more contagious than stretching, yawning has as
respiratory element lacking in stretching,
yawning has a greater involvement of neck and
head structures than stretching, and yawning has
a Valsalva-like (breath holding and "bearing
down") maneuver lacking in stretching.
-
- At present, there is much speculation, but
little evidence about a function for yawning.
However, yawning, like stretching, is a
high-amplitude maneuver that probably has
numerous consequences through the body. Each of
these physiological correlates may be a
"function" (i.e., have some plausible benefit).
There is no evidence that yawning either
increases Or decreases alertness. However,
yawning is linked with some changes in
behavioral states. We yawn during the transition
from sleep to wakefulness, from wakefulness to
sleep, and when becoming bored. The association
between yawning and change in behavioral state
was pointed out by fish behaviorist Arthur
Myrberg (1972), who noticed that when the
damselfish he studied on a reef yawned, they
would soon switch from one to another class of
activity. Yawning may facilitate such state
transitions.
-
- The search for a yawn function should also
consider the phylogerietic antiquity of the act.
Most vertebrates yawn, a fact that indicates a
motor pattern generating process and perhaps at
least one physiological correlate (i.e.,
"function") common to all yawning organisms.
Additional motor components and physiological
correlates may have evolved from this primal
prototype.
-
- The occurrence of yawning during the first
trimester of human prenatal development opens
the possibility of a role of yawning in
embryogenesis. Would it not be surprising if a
function of yawning is to ensure the proper
articulation of the jaw joint by moving it
during development? The sculpting and
maintenance of developing joints is an important
function of prenatal movement (Provirie, 1993b).
Yawn functions noted in contemporary humans,
such as opening the eustachian tube to equalize
pressure in the middle ear and the ambient
environment (Laskiewicz, 1953), may be secondary
consequences of an act evolved in the service of
some other environmental or developmental
challenge.
-
-
- Whatever the physiological and behavioral
consequences of normal yawning, yawning is
symptomatic of a wide range of pathology,
including brain lesions and tumors, hemorrhage,
motion sickness, chorea, and encephalitis
(Graybiel & Knepton, 1976; Jurko & Andy,
1975; Barbizet, 1958; Heusner, 1946). Psychotics
are reported to yawn rarely, except when
suffering from organic brain syndrome (Lchmann,
1979). This intriguing observation, considered
with the finding that antidopinergic agents
often produce yawning, suggests that yawning may
provide a metric for the pathogenesis of
schizophrenia (associated with elevated dopamine
levels) and a useful assay for the titration of
antidopaminergic neuroleptic dosages. Lehmann
(1979) notes further the old clinical
observation that people suffering from acute
physical illnesses never yawn when their
condition is serious; a return of yawning
signals convalesence. In regard to
neurotransmitters, yawning is associated with
cholinergic and peptidergic excitation and
dopaminergic inhibition. Because yawning is
stimulated by hormones (i.e., testosterone,
oxytocin, ACTH, MSH) and drugs (i.e.,
apomorphine, piribedil, pilocarpine) with known
mechanisms of action, yawning can serve as a
useful, noninvasive, behavioral assay of
chemical events within the brain. Clinically,
yawning is therapeutic in preventing atekctasis,
the collapse of alveoli, a frequent
postoperative respiratory complication (Cahill,
1978).
-
- To conclude this discussion of yawning as a
motor act, it is appropriate to return to the
initial ethological theme and review the
properties that qualify yawning as a stereotyped
action pattern (Provine, 1986).
-
- 1. Yawning is species-typical in humans,
performed by all members of our species. [We
do not show the higher rates of male yawning
reported for more dimorphic primates (Schino
& Aureli, 1989).1 Yawning is not, however,
species exclusive; most vertebrates yawn
(Baenninger, 1987; Deputte, 1994; Huesner,
1946).
-
- 2. Yawning is consistent in duration
(average duration 6 s).
-
- 3. Yawning occurs periodically (average
interyawn interval 68 s).
-
- 4. Yawning is under strong genetic control
because it is already performed by embryos
during the first trimester of prenatal
development (DeVries, Visser, & Prechtl,
1982) and is obvious in both normal and
anencephalic human newborns (Heusner, 1946;
Provine, 1989a).
-
- 5. Yawns are unitary, being performed at
so-called "typical intensity." Fractional
(atypically short) yawns are seldom seen.
-
- 6. The amplitude and duration of yawns are
independent of the amplitude of the releasing
stimulus Of present). Further, once initiated,
yawns go to completion with minimal influence of
sensory feedback; everyone is familiar with the
difficulty of trying to stifle a yawn (Provine,
1986).
-
- 7. Yawns can be "released" by witnessing
yawns or yawn-related stimuli (Provine, 1986;
1989b), the basis of the contagious yawn
response.
-
- 8. Yawns are complex in spatiotemporal
organization and have facial, respiratory, and
other components, e.g., yawns are not simple
reflexes of short duration.
-
- 9. The motor components of a yawn occur in
only one order and the timing of components is
consistent from yawn to yawn. This stability of
sequence contributes to fhe yawns unmistakable
appearance, an important property for a
releasing stimulus.
-
- 10. The finding that yawns are prominent in
people who are waiting, or performing monotonous
work (Provine & Hamernik, 1986), and of dogs
on the threshold of aggression, or participating
in an aversive activity, is consistent with the
performance of yawns as "displacement acts"
(Provine, 1986).
-
- Given these many properties, yawning has
been recognized as one of the best examples of
stereotyped action pattern and releasing
stimulus in humans (Alcock, 1989). Yawns are not
reflexes. As traditionally understood, reflexes
are simpler acts of short duration, are evoked
by stimuli, have short response latencies, and
have response amplitudes that are correlated
with stimulus amplitudes.
-
-
- Contagious Yawning
-
-
- The contagiousness of yawning is legendary.
Viewing, reading about, and thinking about
yawning evokes yawns (Provine, 1986). Although
yawning is interesting in its own right,
contagious yawning is a means of assessing the
yawnevoking potency of various facial features.
Thus used, the search for the ethological
releasing stimulus for yawns provides insights
into face detection, an issue in perception and
neuropsychology (Provine, 1989b). The discovery
of a perceptual process activated exclusively by
visually observed yawns establishes a precedent
for a facial feature and/or expression detector
in humans. Similar detectors may exist for
facial expressions (actions) other than yawns,
and for other complex visual stimuli, but their
activity may be more difficult to monitor
because they lack a contagious response as a
behavioral assay.
-
- A series of studies evaluated the
yawn-evoking potency of various features of a
yawning face (Provine, 1986, 1989b). The
yawn-evoking capacity of variations in a 5-min
series of 30 videotaped repetitions of a yawning
face (one yawn every 10 s) were compared with
each other and with a control condition of a
series of 30 videotaped smiles (Provine, 1989b).
Single frames of the monochrome video stimuli in
midyawn or midsmile are shown in Fig. 1. The 360
subjects, 30 per stimulus condition, were
instructed via videotape to observe a video
monitor and to record their yawns by pressing a
button.
-
- The normal yawning face (Fig. la) was an
effective stimulus, causing 16 of 30 subjects
(Fig. 2, upper) to produce a total of 92 yawns
(Fig. 2, lower), significantly more yawns than
to the smile. The yawn-detection process was not
axially specific; yawns in orientations of
90°, 180°, and 270° were as
potent or nearly as potent as normal, upright,
0° yawns. The number of subjects who yawned
in response to the high-contrast yawn (Fig. lb)
did not differ significantly from those who
yawned in response to normal-halftone yawns
(Fig. la) or smiles (Fig. 1h). A tonic (still)
yawn video frame of a yawner in midyawn (Fig.
la) produced a number of yawners midway between,
and not significantly different from that
produced by normal, animate yawns or
smiles.
-
- The "no-mouth" yawn (Fig. le) was the only
stimulus with a deleted feature that produced as
many yawning subjects as the complete face and
significantly more yawners than did the smile
(Fig. 2). This initially counterintuitive and
disconcerting result was, however, consistent
with other data. Consider, for example, the
relative ineffectiveness of the "mouth-only"
yawn (Figs. le and 2). The gaping mouth, the
most obvious candidate for the ethological "sign
stimulus" for yawning, is not necessary to evoke
contagious yawns. Instead, the yawn detector may
be triggered by the overall configuration of the
yawning face, perhaps being driven by cues
involving the squinting of the eyes, tilting of
the head, and movement of the jaw. The
importance of the overall configuration and
dynamic cues in the discrimination of facial
expressions is reinforced by findings of
Leonard, Voeller, and Kuldau (1991). In monkeys,
a lack of axial and feature specificity in many
facespecific neurons suggest a stimulus analysis
of the sort described in the present behavioral
analyses of human yawns (Bruce et al., 1981;
Perrett, Mistlin, & Chitty, 1987; Perrett,
Rolls, & Caan, 1982). Monkeys even have
neurons specific for yawning faces. These
diverse behavioral and neurophysiological
results suggest common underlying processes. It
is unlikely that complex neural mechanisms for
similar perceptual tasks would evolve
independently and have radically different
principles of operation.
-
- Determination of latencies of the contagious
yawn responses provides additional information
about the dynamics and nature of the underlying
process (Provine, 1986). The stimulus in the
latency study was the animate video of the
normal yawning face described previously. As in
the previous experiment, yawns were potent
yawn-inducing stimuli; 23 of 42 subjects (55%)
yawned during a 5-min session. Only 5 of 24
subjects (21%) yawned while viewing the control
condition of a recurrent series of videotaped
smiles. The proportion of subjects yawning while
viewing yawning gradually increased during the
5-min session. These data are consistent with
the involvement of a complex, higher order
perceptual process involving polysynaptic
processes; the contagious yawn mechanism is not
a reflex having a short and consistent
latency.
-
- The complexity of the contagious yawn
mechanism is suggested further by the ariety of
nonvisual stimiIi that can evoke it. As readers
may have concluded already, simply reading about
yawning is sufficient to trigger yawns (Provine,
1986; Carskadon, 1991, l992):The potency of the
text-induced yawning effect was tested
- by comparing the yawns performed by subjects
reading about yawning with yawns performed by
subjects reading a control passage about
hiccupping. Significantly more subjects either
yawned or thought about yawning while reading
about yawning than reading about
hiccupping.
-
- Most stimuli associated with yawning can
evoke yawns. For example, even the sound of
yawning, or thinking or reading about yawning,
triggers yawns. Given the variety of potential
yawn-evoking stimuli, further exploration of the
range of yawn-inducing stimuli may yield
diminishing returns. Although the contagious
yawn is a highly mechanistic social response to
yawn-related stimuli, the underlying process
does not exclusively involve a detector for a
narrowly defined visual stimulus. Does this mean
that the "innate releasing mechanism (IRM)" of
classical ethology is less selective and more
modifiable in humans than in other animals? Or
does the human data inform us of the true nature
of released behavior as performed throughout the
animal kingdom? Our subjective experience of
contagious yawns may provide valuable evidence
that similar released behavior in nonhumans is
not as rigidly determined and selective as is
often assumed.
-
- Age of onset of visually evoked contagious
yawn responses has not been established
(Provine, 1989a). However, spontaneous yawning
is already present by the end of the first
trimester of prenatal development (DeVries et
al., 1982) and is obvious in newborns. In one of
the rare developmental references, Piaget (1951)
suggested that yawning becomes contagious during
the second year of life. Thus, the present
tentative evidence suggests that contagious
yawning develops after the superficially similar
facial-"imitation" response reported in human
neonates (Meltzoff & Moore, 1977, 1983). If
subsequent research confirms this chronology,
the releasing mechanism that triggers contagious
yawns develops and becomes active long after the
motor pattern generator for yawning.
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