Yawning is a primitive yet complex
stereotyped motor response requiring the
concerted activity of facial, oral,
laryngeal, pharyngeal, thoracic, and
abdominal muscles. In humans, yawning may occur
spontaneously, as
commonly seen with infants, or can be
induced by an internal stimulus (e.g. thinking
about yawning) or an
external stimulus (e.g. viewing someone
yawn) referred to as the contagion.
[Provine,[2005]]
The act of
spontaneous yawning is present across many
species, though its function remains unclear.
Conversely,
contagious yawning (CY) has only been
reported in chimpanzees [Anderson et
al.,[2004]] and humans
[Baenninger,[1987];
Lehmann,[1979];
Smith,[1999]],
suggesting a higher level of complexity.
Furthermore,
yawning by contagion likely represents only
a few motor programs, such as contagious
laughter [Provine,
[1996]], which may be
involuntarily induced by external or internal
(in the case of yawning) stimuli, which
have
been well described. [Provine and
Hamernik,[1986]] Despite numerous
theories posited, the underlying etiology
and neurobiology of these contagious motor
programs remain unclear. Current hypotheses on
the evolution of
CY center on its potential role in social
interaction, communication, and the development
of empathy. [Gallese
et al.,[2004];
Lehmann,[1979]; Platek
et al.,[2003],[2005]].
Recent neuroimaging studies of CY, using
blood oxygen level dependent functional magnetic
resonance imaging
(BOLD-fMRI), have shown inconsistent regions
of activation. Noting that experimental
paradigms differed
slightly, the finding of posterior cingulate
and precuneus activations by Platek
et al. [[2005]] suggests that
CY
involves theory of mind (ToM) or empathy
networks, whereas a study by Schurmann
et al. [[2005]] found right
superior temporal sulcus (STS) activation.
Both studies also noted a lack of activation,
during CY, in mirror
neuron areas such as the inferior frontal
cortices when compared with similar
noncontagious motor acts which
did activate mirror neuron areas. The
absence of significant activations in mirror
neuron areas suggests that
highly stereotyped motor patterns, like CY,
do not require true imitation and would
therefore not activate
mirror neurons.
On the basis of these intriguing findings,
we sought to better define the brain regions
activated while subjects
viewed yawn videos when compared with areas
activated while viewing similar noncontagious
facial actions in
an ecologically valid paradigm. We
hypothesized that the viewing of noncontagious
facial analogues to yawning
would activate mirror neurons, whereas the
viewing of contagious yawns would not.
Discussion
To our knowledge, the finding of
ventromedial prefrontal cortex (vmPFC; BA11)
activation associated with the urge to yawn by a
contagion has not been previously reported. Most
commonly, the vmPFC has been shown to assign
relative value to different options, thereby
weighting or biasing future choices and
minimizing decision making time. [Bechara et
al.,[1999],[2000]; Elliott et
al.,[1999]; Fellows and
Farah,[2007]; Northoff et
al.,[2006]] Additional studies have
implicated the vmPFC in empathic processing.
Eslinger [[1998]] noted that
patients sustaining injuries to the prefrontal
cortex developed impairments in empathic
processing, thereby limiting their capacity to
process emotional information. Similarly,
Shamay-Tsoory et al. used empathy scores and ToM
tasks to study brain injured patients with
frontal lesions, posterior lesions, and controls
to assess whether changes in empathic processing
correlated with particular structural lesions.
They found activity in the right ventromedial
prefrontal cortex to correlate highly with
impairments on various empathy measures.
[Shamay-Tsoory et al.,[2003]]
Functional imaging studies have also implicated
vmPFC and orbitofrontal regions in ToM tasks.
[Baron-Cohen et al.,[1994]; Calder
et al.,[2002]; Fletcher et
al.,[1995]; Gallagher et al.,[2000)
Goel et al.,[1995]].
Our finding of vmPFC activation therefore
suggests that this area may be the prefrontal
component of the empathy network, which has been
previously implicated in CY. In addition to the
finding of vmPFC activation associated with CY,
our results provide a basis on which to
integrate the discrepant findings of Platek et
al. [[2005]] and Schurmann et
al. [[2005]]. We found similar
activation of parahippocampal/ventral posterior
cingulate areas identified by Platek et al.,
although we found no significant activations in
the precuneus or thalamus. These regional
similarities did not, however, differ between
our yawn and gape conditions. Our paradigm also
showed activation of what has been indirectly
shown to be the human mirror neuron system
[Buccino et al.,[2001]; Carr et
al.,[2003]; Leslie et
al.,[2004]; Rizzolatti
and Craighero,[2004]], including
inferior frontal gyrus and STS in both the cough
and gape conditions, in addition to right
ventral premotor, pre-SMA, and inferior parietal
lobule in the gape condition. When contrasting
yawn vs. gape, we found no significant mirror
neuron activations, because this region was
active in both conditions as well as the cough
condition at subthreshold levels.
These findings thereby support the results
of Schurmann et al. [[2005]] and
further suggest that although the right premotor
cortex may be involved with the processing of
facial expressions, it is not unique to yawning
and is not likely to be the primary region
underlying contagious motor programs. The
mechanism by which a contagion releases a yawn
remains unclear.
[Provine,[2005]] The involvement
of vmPFC in the urge to yawn by contagion is
however underscored by this region's association
with emotional processing of internal and
external stimuli and representation of emotional
responses. [Bush et al.,[2000]; Lane
et al.,[1997];
Posner,[1995]] Furthermore, although
the motor act of yawning does not require
cortical control, our findings suggest that the
cortex may be required for transmittal of a
contagious motor program like yawning. The vmPFC
thus appears an ideal region for processing and
releasing contagious motor programs. It may also
help to explain how the urge to yawn by a
contagion could be unique to humans and possibly
nonhuman primates, although spontaneous yawning
is present even in lower animals.
This proposed role of the vmPFC may also
provide insights to explain the early
observations of Piaget [[1951]]
and the recent work of Anderson
and Meno [[2003]] noting CY did
not develop in children below 5 years of age. It
remains unclear, however, what developmental or
biological milestones (e.g., axonal myelination,
synaptic plasticity, empathic processing) must
take place in the child's brain before motor
programs can be released via a contagion. These
findings are in contradistinction to the
paradoxical innate capacity to imitate which is
present in healthy human neonates.
[Nagy,[2006]] Further studies
are needed to identify whether contagious and
noncontagious motor programs are processed by
different neural correlates in order to develop
a unified framework, which accounts for both the
current view that CY has evolved as a form of
empathic modeling and that the mirror neuron
system is the primary substrate for experiential
or empathic understanding of others.
Although our findings identify a new
component to the network underlying CY, we
acknowledge that only eight (47%) of our 17
naïve subjects, who reported experiencing
CY in general, reported feeling a similar urge
during the experiment and suppressing it. For
comparison, Provine [[1989]]
reported subjects' yawn response rates of 55%
during the viewing of a 5 min series of 30 yawns
versus 21% who yawned while viewing a series of
smiles. With regard to the potential confound
introduced by suppression of yawning which
exists in similar experiments, our post hoc
results suggest that the vmPFC was not
associated with suppression and also identifies
regions such as the anterior cingulate, which
are known to be active during cognitive and
motor suppression [Bush et
al.,[2000]; Krams et
al.,[1998]].
Based on these collective data, the highly
evolved vmPFC appears a valid brain region for
the processing and release of contagious motor
programs such as yawning. Taken together, these
data suggest that the urge to yawn via
contagion, unlike other noncontagious facial
expressions, does not take place through a
process of imitation or mimicry, rather the
primitive motor program is released by the
cortex and is carried out through
well-characterized brainstem and subcortical
mechanisms.
