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Echokinetic yawning, theory of mind, and empathy Humans are social beings. One of the pri- temporal region (IT) allows immediate overall mordial functions of the brain is to enable optimal recognition of faces, both their identity and their interaction with others. The success of social inter- expression, apparently through its own autono- action resides in the capacity to understand others mous, non-hippocampal memory (4). As for the in terms of motor actions (intentionality), emotio- superior temporal sulcus (STS), it is specifically acti- nal perception, and a mnemic and comparative vated during perception of eye and mouth move- cognitive integration which separates the self from ments, which suggests its implication in the visual others (empathy, altruism). In psychology, all the- perception of emotions, once again by the activa- se capacities are referred to collectively as Theory tion of mirror neurons. These neurons mime the expres- of Mind (TOM). It has long been known that yaw- sion perceived, helping the observer to understand ning is "contagious"; ethologists speak of beha- it. Schürmann et al. (2) demonstrated that the STS vioural imitation and neurologists refer to echoki- is activated during echokinetic yawning. This acti- nesis, a term coined by JM. Charcot. How does vation, automatic and involuntarily, is transmitted such echokinesis turn yawning into a form of non- to the left amygdala, the posterior cingulate cortex verbal social communication related to TOM and and the precuneus. These structures are thought to empathy? play a role in differentiating emotions expressed by The discovery of mirror neurons by the human face and, especially, in evaluating the Rizzolatti and Gallese (1) offers a neurophysiolo- sincerity of the sentiment expressed. gical explanation for TOM. In most vertebrates, Using fMRI, Platek et al. (5) found a cor- developing the capacity to explore the environ- relation between personality traits and the activa- ment, making decisions (especially in a life-or- tion of neuronal circuits beyond the STS. « In death response to a predator) and general preparation contrast to those that were unaffected by seeing for action involve the activation of these mirror someone yawn, people who showed contagions neurons, along with motor neurons, in cortical yawing identified their own faces faster, did bet- motor areas. Mirror neurons are activated when ter at making inferences about memal states, and the movements and actions of conspecifics are per- exhibited fewer schizotypal personality characte- ceived, indicating that intentional action and the cor- ristics. These results suggest that contagious yaw- responding mental imagery share the same neuro- ning might be related to selfawareness and empa- nal structures. Hence, when a single pigeon senses thic processing »(6). Subjects considered the approach of a pedestrian, the entire flock auto- empathetic, who were very susceptible to echoki- matically flies away, even though most of the birds netic yawning, activated the amygdala and the cin- did not actually perceive the danger. This coope- gulate cortex, whereas schizotypal subjects, who rative motor automatism is a result of adaptive res- were not susceptible to this type of yawning, did ponses selected by evolution. It serves the group not activate these structures. Neurophysiological stu- by providing protection from predators. dies of empathy (7) show similar zones of activa- Echokinesis-induced yawning does not correspond tion (STS, insula, amygdala, cingulate cortex). to this mechanism, as indicated by its latent appea- These data imply that contagious yawning may rance and its inconsistency. In fact, echokinesis reside in brain substrates which have been impli- only occurs in situations of minimal mental sti- cated in self-recognition and mental state attribu- mulation (public transport); during prolonged intel- lion, namely the right prefrontal cortex. lectual effort, people are not susceptible to this During echokinetic yawning, frontal lobes phenomenon. Using functional MRI (fMRI), show no inhibitor activity. Therefore, it appears Schürmann et al. (2) confirmed that during echo- that while the understanding of intentionality kinetic yawning, there is no activation of mirror neu- (motor mirror neurons) and the sharing of the emo- rons in motor areas of the human brain (left pos- tions (mirror neurons in the insula, amygdala and terior inferior frontal cortex), whereas these neurons right parietal cortex) require a common action-per- are activated during observation of other types of ception neuronal activation and, simultaneously, facial gestures (decoding of intentionality). These frontal inhibition (orbitofrontal activation) to pre- ethological and neurophysiological elements vent motor exteriorisation, echokinetic yawning demonstrate that, strictly speaking, echokinetic cannot be inhibited involuntarily due to the poten- yawning is not motor imitation. tially absence of frontal inhibiting relays. In Visual recognition of one's environment contrast, the right temporoparietal activation makes involves various neuronal circuits which distin- it possible to differentiate between the self and guish inanimate objects from living creatures (3). others, and thus identify on a conscious level that Recognition of human faces involves specific dedi- another person's yawn has acted as a trigger (8). Yawning cated neurons in the temporal area. The inferior could thus illustrate the simulation theory of mind. 1 Whereas yawning is universal amongst 2 - Schürmann M, Hesse MD, Stephan KE, et al. vertebrates, it appears that only primates are Yearning to yawn: the neural basis of contagious capable of echokinetic yawning. Anderson (9) yawning. Neuroimage. 2005;24:1260-1264. reported that chimpanzees yawn while watching a video of their conspecifics yawning, but not whi- 3 - Puce A, Perrett D. Electrophysiology and brain le watching other facial expressions. Chimpanzees imaging of biological motion. Philos Trans R Soc thus appear to be susceptible to echokinetic yaw- Lond B Biol Sci. 2003;358:435-445. ning in the same way humans are. Although the existence of a TOM in chimpanzees remains 4 - Afraz SR, Kiani R, Esteky H. Microstimulation controversial (10), the observation of echokinetic of inferotemporal cortex influences face categori- yawning in this species argues in favour of diffe- zation. Nature. 2006;442:692-695. rent levels of TOM, which are perhaps secondary to the different evolutionary paths of cognitive 5 - Platek SM, Mohamed FB, Gallup GG Jr. development in hominids. Human psychiatric Contagious yawning and the brain. Brain Res Cogn pathology also dissects TOM in a similar way (11). Brain Res. 2005;23:448-452. Senju et al. showed video clips of people either yawning or simply opening and closing their 6 - Platek SM, Critton SR, Myers TE, Gallup GG. mouths to 49 children who were 7 years or older, Contagious yawning: the role of self-awareness half of whom were autistic. The yawning faces and mental state attribution. Brain Res Cogn Brain triggered more than twice as many yawns in non- Res. 2003;17(2):223-237. autistic children than in their autistic counterparts. This study suggests that contagious yawning is 7 - Carr L, Iacoboni M, Dubeau MC, et al. Neural impaired in autism spectrum disorders, which mechanisms of empathy in humans: a relay from may relate to their impairment in empathy (14). neural systems for imitation to limbic areas. Proc Anderson (12) showed that children were Natl Acad Sci USA. 2003;100:5497-5502. only susceptible to echokinesis-induced yawning during their sixth year, i.e. after acquiring the abi- 8 - Decety J, Grezes J. The power of simulation: lity to reflect on what others are thinking and attri- imagining one's own and other's behavior. Brain Res. bute mental states accordingly. In other words, one 2006;1079:4-14. must possess a state of cognitive maturity on a functional level to be susceptible to echokinetic 9 - Anderson JR, Myowa-Yamakoshi M, yawning. Consequently, there is a phenomenolo- Matsuzawa T. Contagious yawning in chimpan- gical link between the capacity to attribute mental zees. Proc Biol Sci. 2004;271 Suppl 6:S468-470. states to others (TOM), which is the basis for empa- thy, and what is commonly referred to as contagious 10 - Povinelli DJ, Vonk J. Chimpanzee minds: sus- yawning. In addition to the neuroanatomical hie- piciously human? Trends Cogn Sci. 2003;7:157-160. rarchy separating TOM into sensorimotor, emo- tional and cognitive levels, echokinetic yawning 11 - Blair RJ. Responding to the emotions of others: makes it possible to disassociate TOM, via its onto- dissociating forms of empathy through the study of genesis and its phylogenesis, into various deve- typical and psychiatric populations. Conscious lopmental levels, an approach which is reinforced Cogn. 2005;14:698-718. by the differential activation of specific neuronal circuits (13). This type of yawning may have 12 - Anderson JR, Meno P. Psychological conferred a selective advantage by synchronising influences on yawning in children. Current the level of vigilance between the members of a social Psychology Letters Behaviour, Brain, & Cognition. group. It may also take part in a form of involun- 2003;2:390. tary instinctive empathy, which could be qualified as rudimentary and probably appeared late in the 13 - Singer T. The neuronal basis and ontogeny of course of hominid evolution (in the neomammalian empathy and mind reading: Review of literature brain proposed by P. McLean). and implications for future research. Neurosci Biobehav Rev. 2006;30:855-863. 1 - Rizzolatti G, Fadiga L, Gallese V, et al. 14 - Senju A, Maeda M, Kikuchi Y et al. Absence Premotor cortex and the recognition of motor of contagious yawning in children with autism actions. Brain Res Cogn Brain Res. 1996;3:131-141. spectrum disorder. Biology letters 2007; in press. 2
"Echokinetic yawning theory of mind and empathy"