mise à jour du
26 octobre 2008
Human Brain Mapping
Contagious yawning and the frontal lobe:
An fMRI study
Fatta B. Nahab , Noriaki Hattori, Ziad S. Saad, Mark Hallett
Human Motor Control
National Institutes of Neurological Disorders and Stroke
National Institutes of Health, Bethesda, Maryland, USA


Tous les articles sur la contagion du bâillement
All articles about contagious yawning
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.
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.