Ongoing debate in the literature concerns
whether there is a link between contagious
yawning and the human mirror neuron system
(hMNS). One way of examining this issue is with
the use of the electroencephalogram (EEG) to
measure changes in mu activation during the
observation of yawns. Mu oscillations are seen
in the alpha bandwidth of the EEG (8-12 Hz) over
sensorimotor areas. Previous work has shown that
mu suppression is a useful index of hMNS
activation and is sensitive to individual
differences in empathy. In two experiments, we
presented participants with videos of either
people yawning or control stimuli. We found
greater mu suppression for yawns than for
controls over right motor and premotor areas,
particularly for those scoring higher on traits
of empathy. In a third experiment, auditory
recordings of yawns were compared against
electronically scrambled versions of the same
yawns. We observed greater mu suppression for
yawns than for the controls over right lateral
premotor areas. Again, these findings were
driven by those scoring highly on empathy. The
results from these experiments support the
notion that the hMNS is involved in contagious
yawning, emphasise the link between contagious
yawning and empathy, and stress the importance
of good control stimuli.
These are interesting times for a field
concerned with a physiological process often
associated with boredom, namely yawning. In
particular, the study of contagious yawning
appears to offer a fruitful avenue of
investigation for the growing fields of
developmental, affective, and social
neuroscience. Contagious yawning refers to the
phenomenon wherein seeing or hearing someone
yawn, or even reading or thinking about yawning,
can trigger a yawn in the beholder (Platek,
Mohamed, & Gallup, 2005). It typically
occurs in 40%-60% of the population (Platek,
Critton, Myers, & Gallup, 2003; Provine,
1989), which begs the question, what underlies
the individual differences in this phenomenon?
To date, much of the evidence points to a link
between contagious yawning and the level of
empathy of the individual (Platek, 2010; Platek
et al., 2003; Platek et al., 2005;
Schürmann et al., 2005; Senju et al.,
2007). Indeed, clinical populations who
typically exhibit impairments in empathic
processing (e.g., schizophrenia and the autism
spectrum disorders, or ASD) also demonstrate a
paucity of contagious yawning under normal
circumstances (Haker & Rossler, 2009; Senju
et al., 2007), but in the case of ASD, this can
be rectified given instructions to fixate on the
eyes of the person yawning (Senju et al.,
2009).
One of the main candidate mechanisms for
empathic processing in general is the mirror
neuron system. Mirror neurons were originally
observed in monkeys and are a specific type of
motor cell that fires not only when the animal
makes a specific movement, but also when it
observes the same movement being carried out (di
Pellegrino, Fadiga, Fogassi, Gallese, &
Rizzolatti, 1992; Gallese, Fadiga, Fogassi,
& Rizzolatti, 1996). Since these original
observations, a multitude of studies have
examined human correlates of such activation
using indirect methods such as fMRI,
electroencephalograms (EEGs), or transcranial
magnetic stimulation, and these studies have
predominantly shown that such a mechanism (often
referred to as the human mirror neuron system;
hMNS) exists in humans. A recent study using
single-cell recording in humans claims to have
found the first direct evidence for the
existence of mirror neurons per se in humans
(Mukamel, Ekstrom, Kaplan, Iacoboni, &
Fried, 2010). It has been postulated thatmirror
neurons may underlie many social skills, such as
action understanding, imitation, theory of mind,
language, and empathy (Rizzolatti &
Craighero, 2004). With regard to empathy,
several studies have demonstrated a correlation
between it and hMNS activation. For instance,
Kaplan and Iacoboni (2006) presented hand
stimuli in various conditions designed to
contrast intentional aspects of the scene and
observed BOLD activation in the right inferior
hMNS that correlated with empathic concern on
the Interpersonal Reactivity Index (IRI; Davis,
1983). Using an auditory paradigm, Gazzola,
Aziz-Zadeh, and Keysers (2006) found a
correlation between hMNS activation to the
sounds of actions and the Perspective Taking
subscale of the IRI, and when observing and
imitating emotional facial expressions, Pfeifer,
Iacoboni, Mazziotta, and Dapretto (2008) found
that frontal hMNS activity correlated with both
empathic behaviour and interpersonal skills. It
has also been hypothesised that a faulty hMNS
may underlie many of the social deficits
(including empathy) observed in ASD (Martineau,
Andersson, Barthélémy, Cottier,
& Destrieux, 2010; Oberman et al., 2005;
Ramachandran & Oberman, 2006) and
schizophrenia (Enticott et al., 2008), and may
account for the individual differences in
autistic traits observed in the general
population (Puzzo, Cooper, Vetter, & Russo,
2010).
Given this putative link between empathy and
the hMNS and the deficits in both contagious
yawning and empathic skills observed in ASD and
schizophrenia, it would not appear unreasonable
to speculate that the hMNS may indeed be
involved in contagious yawning (Cooper, Puzzo,
& Pawley, 2008). However, the neuroimaging
evidence to date is less than convincing, and
consequently there is disagreement in the
literature as to whether or not the hMNS is an
important factor in contagious yawning.
Generally, neuroimaging research on contagious
yawning depends crucially on the design of the
control conditions. For instance, Platek et al.
(2005), when comparing fMRI BOLD signals between
participants observing yawns or laughs, observed
unique activation to yawns in the precuneus and
posterior cingulate areas associated with
empathic processing, but which are not part of
the hMNS. However, given the socially contagious
nature of laughter, the use of laughs as a
control stimulus may have masked any
contribution of the hMNS to contagious yawns.
Schürmann et al. (2005) using a video of a
"nonnameable mouth-andtongue" action as a
control condition, found activation to yawns in
the right posterior superior temporal sulcus
(STS) and bilaterally in the anterior STS, but
not in frontal hMNS areas. The authors proposed
that this indicates that contagious yawning does
not require the detailed action understanding
afforded by the hMNS. However, it should be
noted that STS is considered by some to be a
part of the extended mirror neuron system,
although not a core area (Pineda, 2008), since
it contains cells that are involved in coding
biological motion (Jellema, Baker, Oram, &
Perrett, 2002). More recently, Nahab and
colleagues used fMRI to examine reactivity to
yawn stimuli in comparison to three control
stimuli: a still face, a cough, and a gape
(Nahab, 2010; Nahab, Hattori, Saad, &
Hallett, 2009). Unique activation to yawns was
observed in the ventromedial prefrontal cortex,
which was positively correlated with the urge to
yawn; activation common to all stimuli was noted
in hMNS areas. The only neuroimaging study to
date to find evidence of specific hMNS
involvement in contagious yawning has come from
Arnott, Singhal, and Goodale (2009). Using an
auditory paradigm, they contrasted the sound of
yawns with electronically scrambled versions of
the same stimuli. In this context, greater BOLD
activation to yawns was observed in the right
inferior frontal gyrus (a core area of the
hMNS), and this activation was greatest for
stimuli associated with high ratings for an urge
to yawn.
Consequently, we undertook a series of
experiments in an attempt to address the
discrepancies between these neuroimaging
investigations of contagious yawning. The EEG
was our psychophysiological tool of choice, as
it affords both a much higher temporal
resolution than fMRI, as well as a readily
identifiable index of hMNS
activation&emdash;namely, mu suppression. Mu
suppression (or mu event-related
desynchronisation, ERD) refers to a decrease in
power in the alpha (8-12 Hz) and sometimes the
lower beta (12-20 Hz) bandwidths of the EEG over
sensorimotor areas relative to a reference
interval; an increase in mu power is referred to
as event-related synchronisation, or ERS. In
this article, we will use the terms mu
suppression and alpha ERD (over sensorimotor
areas) interchangeably. ERD is observed during
motor acts (Arroyo et al., 1993; Chatrian,
Petersen, & Lazarte, 1959; Gastaut, 1952),
during preparation for action (Jasper &
Penfield, 1949), while imagining a movement
(Pfurtscheller, Neuper, Brunner, & da Silva,
2005), and, pertinent to the present study,
while observing a movement (Gastaut & Bert,
1954; Hari et al., 1998; Kilner, Marchant, &
Frith, 2009; Muthukumaraswamy & Johnson,
2004; Pineda, 2005; Streltsova, Berchio,
Gallese, & Umiltà, 2010). As a
result, mu suppression has been posited to be a
useful indicator of action observation pattern
matching in the cortex, and at present, the best
candidate area for this process appears to be
the hMNS. Indeed, mu suppression to various hand
movements has been shown to closely mirror BOLD
activation in areas analogous in humans to the
mirror neuron areas in primate studies (Perry
& Bentin, 2009); to be modulated by the
laterality of the presentation stimulus,
consistent with the reactivity of mirror neurons
in area F5 in monkeys (Kilner et al., 2009); and
to be dynamically modulated similarly in both
action observation and action performance
(Press, Cook, Blakemore, & Kilner, 2011).
Consequently, mu suppression during action
observation is usually interpreted as an index
of activity in the hMNS (Kilner et al., 2009;
Pineda, 2005, 2008). Indeed, whereas until
recently, mu suppression during action
observation has been postulated to result from
postsynaptic modulation from mirror neurons in
premotor cortex (Pineda, 2008; Rizzolatti &
Craighero, 2004), recent evidence for socalled
M1 view cells in primary motor cortex with
mirrorneuron- like properties (Dushanova &
Donoghue, 2010) suggests that perhaps mu
suppression may be a more direct measure of hMNS
than was previously believed, as M1 may itself
be a part of the mirror neuron system (Press et
al., 2011). Given the proposed multimodal nature
of hMNS activity, we decided to examine the
possible link between it and contagious yawning
using both visual and auditory protocols. In
Experiments 1 and 2, we used visually presented
videos of yawns and gapes. Then, Experiment 3
was a constructive replication of Arnott et al.
(2009) using auditory stimuli. Given Arnott et
al.'s findings of right inferior frontal hMNS
activation during yawns, we focused our analyses
on analogous areas (i.e., the right FC and C
electrode strips). We hypothesised that yawn
stimuli would elicit greatermu suppression than
would control (non-yawn) stimuli. We were also
interested in the possible links between
empathy, contagious yawning, and mirror neurons,
and so we also hypothesised that mu suppression
would be greater for those scoring high on a
measure of empathy (the IRI) and that this
effect would be greater during yawns than during
nonyawns.
....
General discussion
In three experiments, in line with our
predictions, we demonstrated greater mu
suppression over right frontocentral areas when
participants were exposed to yawns as opposed to
control stimuli. We also noted that those who
score highly on measures of empathy tend to
exhibit greater suppression of their ongoing mu
activity than do those with low scores, and that
this appears to be particularly evident during
yawn stimuli. Similarly, we observed with an
increase in autistic traits, a corresponding
decrease in mu suppression (less
desynchronisation), and we suggest that this
effect may underlie the decrease in contagious
yawning noted in ASD (Senju et al., 2007). In
the context of action observation, mu
suppression is regarded as a reliable index of
mirror neuron activation (Kilner et al., 2009;
Muthukumaraswamy & Johnson, 2004; Pineda,
2005, 2008). Consequently, the parsimonious
interpretation of our data is that the human
mirror neuron system (hMNS) is activated when
observing yawns, and we suggest that this system
may underlie the contagious aspects of the
phenomenon. This interpretation is in accordance
with Arnott et al. (2009), who found increased
BOLD activation to the sound of yawns in right
inferior frontal gyrus (a core component of the
hMNS), but not with three other neuroimaging
studies, which found no evidence for hMNS
activation during contagious yawning above that
found during exposure to control stimuli (Nahab
et al., 2009; Platek et al., 2005;
Schürmann et al., 2005). We propose three
possible reasons why those studies might have
failed to find hMNS involvement in contagious
yawning: Firstly, EEG provides a different
method for investigating cortical activation to
yawn stimuli (i.e., neural synchrony, as opposed
to changes in blood oxygen levels); secondly,
the control stimuli used were also likely to
activate hMNS, and therefore might have obscured
the results; thirdly, individual differences in
personality traits such as levels of empathy
were not built in to the studies' factorial
designs.
In the present study, the findings of
greater mu suppression during exposure to yawn
stimuli for those who score highly on measures
of empathy fit well with the previous literature
linking contagious yawning with empathy (Platek
et al., 2003; Senju et al., 2007), and also with
studies correlating empathy with hMNS activation
(e.g., Gazzola et al., 2006; Kaplan &
Iacoboni, 2006; Pfeifer et al., 2008). This is
particularly so for the low alpha band over
right frontal areas during the later part of the
stimulus presentation, where this effect was
found first in Experiment 1 and was replicated
in Experiment 3. Thus, both experiments that
examined empathy observed this effect. Despite
the support for our hypotheses that our data
provide, some limitations do need to be
acknowledged. For instance, not all of the
findings from Experiment 1 were replicated in
the later experiments. For example, the near
significant (p 0 .05) finding of greater
upper-alpha ERD to yawns than to controls over
right central electrodes during the early part
of the video presentation was not found again.
However, a similar effect in the later part of
the video presentation was replicated in
Experiment 2. Clearly, other significant effects
found in Experiment 1 pertaining to individual
levels in empathy would not be expected to be
observed in Experiment 2 (where empathy was not
measured). Additionally, in Experiment 3, a
median split for empathic concern was used to
divide the data, and so would have had less
power than creating groups based on separations
of one standard deviation from the mean (as in
Exp. 1), and therefore the failure to replicate
findings may be attributable to this.
Furthermore, differences in the findings between
the three experiments may also have resulted
from differences in experimental modality (e.g.,
visual vs. auditory stimuli).We are also aware
that the control stimuli we used were still not
optimal and might have also activated hMNS
(albeit to a lesser extent than the yawn
stimuli); this might have diluted our findings.
The creation of a definitive control condition
for yawns remains a high priority for
researchers in this field. It is also important
to consider the possibility that the observed mu
suppression might have been caused by mechanisms
other than hMNS. For instance, if networks
involved in other social cognition skills (e.g.,
theory of mind) created a motor command to yawn
in response to observing a yawn, this, too,
would excite the motor cortex, leading to a
desynchronisation of mu activity. Indeed, given
that various theory-of-mind behaviours
(especially with regard to affect) have recently
been associated with activation of the
ventromedial prefrontal cortex (vmPFC; Abu-Akel
& Shamay-Tsoory, 2011; Lev-Ran, Shamay-
Tsoory, Zangen, & Levkovitz, in press), such
an explanation could bind our results in the
present study with those of Nahab et al. (2009),
who found vmPFC activation to yawn observation.
Additionally, it has recently been argued that
hMNS and non-mirror theory-of-mind networks work
together in a complementary fashion to
facilitate the understanding of actions (de
Lange, Spronk, Willems, Toni, & Bekkering,
2008; Schippers, Roebroeck, Renken, Nanetti,
& Keysers, 2010); future work on contagious
yawning should explore this possibility.
However, to date, and to the best of our
knowledge, no such link between vmPFC andmotor
cortex activation has been reported in this
context, and the most widely published
explanation of mu suppression to observation of
an action is downstream modulation of motor
cortex by premotor mirror neurons (Pineda, 2008;
Rizzolatti & Craighero, 2004), although
recently, direct mirror-neuron-like activity has
been observed in M1 itself (Dushanova &
Donoghue, 2010; Press et al., 2011). Therefore,
at present, the most plausible explanation of
our data is in terms of hMNS activation during
the observation of yawns, but this should not
preclude the investigation of a possible link
between vmPFC and hMNS in future studies.
In summary, we have presented evidence of
greater mu suppression to observing yawn stimuli
than to observing control stimuli. Given an
interpretation of the desynchronisation of mu
power as a putative index of hMNS activation,
our results are consistent with previous
findings by Arnott et al. (2009) implicating the
human mirror neuron system in the phenomenon of
contagious yawning. This is particularly
apparent when controlling for individual
differences in empathic abilities. Future
studies in this field will need to take these
findings into account and also to design control
stimuli that do not activate the hMNS.
