Saturday, January 7, 2012

Contagious Yawning from Human to Domestic Dogs: Is It Possible? What Are The Implications?

Yawning is a phenomenon that occurs not only in human but also in other animals such as mammals, fishes, amphibians, reptiles and birds (Heusner, 1946; Baenninger, 1987; Gallup et al., 2009). There are many proposed reasons and functions as to what elicit yawning behavior in an individual but little is known about the role of contagious yawning and how animals can catch yawns from other species. Even though yawning is widespread in the animal kingdom, contagious yawning has only been reported in humans, chimpanzees (Pan troglodytes), stumptail macaques (Macaca arctoides) and recently in domestic dogs (Canis familiaris) (Provine, 1986; Platek et al., 2003; Anderson et al., 2004; Paukner & Anderson 2006; Joly-Mascheroni et al., 2008; Harr et al., 2008). In addition, studies have shown that there is a positive correlation in the susceptibility of contagious yawning with empathy and theory of mind (Platek et al., 2003; Preston & de Waal, 2002), and that emotional closeness and relatedness between an individual is key to eliciting contagious yawning in human (Norscia & Palagi, 2011).

Contagious yawning has been reported in humans, chimpanzees, stumptail macaques and  domestic dogs.
There have been many suggestions on the roles of contagious yawning, especially in primates. Some literatures hypothesized that contagious yawning in primates plays potential roles in communication, social interaction, empathy and self-awareness (Deputte, 1994; Daquin et al., 2001; Platek et al., 2003; Gallese et al., 2004; Platek et al. 2005) while others thinks that it is a stereotyped action behavior and an innate releasing mechanism (Provine, 1986). In addition, Platek et al. (2003) showed a positive correlation in the susceptibility to contagious yawning with self-face recognition and theory of mind stories while children with autism spectrum disorder showed an absence in contagious yawning (Senju et al., 2007) suggests that contagious yawning may be related to empathy (Preston & de Waal, 2002). A recent study on yawn contagion in human shows that related individuals (r ≥ 0.25) were the ones that are more susceptible to contagious yawning, and concludes that emotional closeness between an individual is key to contagious yawning in human as opposed to other variable such as sex or country of origin (Norscia & Palagi, 2011).

Although yawning is widespread in the animal kingdom, contagious yawning has only been reported in humans (Provine, 1986; Platek et al., 2003), chimpanzees (Anderson et al., 2004), stumptail macaques (Paukner & Anderson 2006) and domestic dogs (Joly-Mascheroni et al., 2008; Harr et al., 2008). Contagious yawning from human to domestic dogs  is interesting because it could further elucidate if empathy was inadvertently selected for in domestic dogs as they evolve side by side with modern humans. If yawns can indeed be passed from human to domestic dogs, we can posit that domestic dogs are capable of empathy. Further experiment on contagious yawning from the owner (human) to domestic dogs could also elucidate whether yawns are more susceptible based on emotional closeness as per Norscia & Palagi's (2011) research, albeit their subjects are all humans.

Neonatal macaque imitation the expression of a researcher.
Gallese et al. (2004) contended to the fact that mirror neurons play an integral part on the theory of mind and empathy. Later experiment by Iacoboni et al. (2005) posits that mirror neurons are involved in understanding the intention of others. By using an FMRI, human subjects were exposed to 3 types of stimuli on 24 second video clips. These stimuli show grasping hand action without a context (Action), context-only (Context), and grasping hand with and without context (Intention). In the Action stimuli, a hand was shown grasping a cup in the absence of context and an objectless background. Two types of grasping actions were used: either precision grasping (hand grasping the cup handle) or whole-hand grasping (hand grasping the cup body). The Context stimuli showed three dimensional objects such as a teapot, a mug or a cookie just before or just after having tea to elicit a drinking or cleaning context. For the Intention stimuli, the subjects were presented with both grasping actions in both drinking and cleaning context. When presented with the Intention stimuli, there is a significant signal increase in the premotor cortex; the posterior part of the inferior frontal gyrus and the adjacent sector of the ventral premotor cortex where hand actions are represented. The authors argue that the premotor mirror neuron areas are involved in understanding the intention of others, evident from a spike of signal in the FMRI when humans were exposed to Intention stimuli in the experiment.

Other experiments have shown that in pigtailed macaques, Macaca nemestrina, mirror neurons are also found in the inferior frontal gyrus (the F5 region). This region responded when the macaques make an active movements and also when they observe an experimenter making meaningful movements. (di Pellegrino et al., 1992; Gallese et al., 1996; Rizzolatti & Craighero, 2004; Hickok, 2009).

In a study by Platek et al. (2005), the authors found that the posterior cingulate and precuneus were activated during contagious yawning. These two regions are associated with the theory of mind and empathy. In another study from the same year, Schürmann et al. (2005) found that the superior temporal sulcus was the area that gets activated during contagious yawning. The superior temporal sulcus region is involved in the perception of eye gaze of others and are crucial in determining where others’ emotion are being directed through eye gaze (Campbell et al., 1990). Thus, neuroimaging results from Platek et al. (2005) and Schürmann et al. (2005) contradict each other in isolating the region of the brain that is activated during contagious yawning.

Two studies on contagious yawning from human to domestic dogs were published by Joly-Mascheroni et al. (2008) and Harr et al. (2008) in the same year. Joly-Mascheroni et al. (2008) were the first to demonstrate that human yawns are contagious to domestic dogs and that human yawns would elicit a yawning response from a non-primate species (domestic dog). In this ingenious experiment, Joly-Mascheroni et al. (2008) had 29 domestic dogs observed human yawning and making control mouth movements (not yawns). Out of the 29 domestic dogs, 21 of them yawned after observing a human yawning but none when exposed to control mouth movements (the control in the study). The experiment yielded impressive result, where 72% of the domestic dogs yawned when exposed to a human yawning. This is a higher rate than contagious yawning between humans (45% – 60%) (Provine, 1986; Platek et al., 2003) and from human to chimpanzee (33%) (Anderson et al., 2004). Joly-Mascheroni et al. (2008) posit from this experiment that domestic dogs possess a rudimentary empathic capability and that it helps in moderating human-dog interaction and communication.

A later study by Harr et al. (2008) in the same year also investigated whether human yawns are contagious to domestic dogs but used a different method than that of Joly-Mascheroni et al. (2008). Harr et al. (2008) used 15 domestic dogs in their experiment; the domestic dogs were shown video clips of humans and domestic dogs displaying yawns and open mouth expressions (not yawns) to determine whether these two social stimuli would elicit yawning in these domestic dogs. Their results show that the domestic dogs yawned on both stimuli (yawn and open mouth expressions) with no significant difference as determined by paired t test. Citing methodological difference than that of Joly-Mascheroni et al. (2008), Harr et al. (2008) posit that their results were due to using video clips instead of using live human models. They also conclude that it is possible that domestic dogs, like humans, attended differently to video stimuli than that of a live model.

Järveläinen et al. (2001) showed that in humans, there is a stronger reactivity time in the mirror neuron system when viewing live motor act than that of an artificially presented act. It is possible that domestic dogs also pay less attention to an artificially presented act than that of a live motor act. Understanding the umwelt of domestic dogs is important when using them as experimental subjects and to answer species-specific questions. Domestic dogs are excellent at reading human communicative and visual cues (Joly-Mascheroni et al., 2008) but maybe only so on live model and not video clips as evident from Harr et al. (2008) experiment. Thus, experiment on contagious yawning from human to domestic dogs should considering using only live models and not video clips.

P/S - Sorry if I made you yawn ;)


Anderson, J. R., Myowa-Yamakoshi, M., & Matsuzawa, T. (2004). Contagious yawning in chimpanzees. Proc. R. Soc. B, 271(Suppl. 6), S468–S470.

Baenninger, R. (1987). Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. J. Comp. Psychol. 101, 349–354.

Campbell, R., Heywood, C.A., Cowey, A., Regard, M., & Landis, T. (1990). Sensitivity to eye gaze in prosopagnosic patients and monkeys with superior temporal sulcus ablation. Neuropsychologia, 28(11), 1123-1142.

Daquin, G., Micallef, J. & Blin, O. (2001). Yawning. Sleep Med. Rev. 5, 299–312.

Deputte, B. L. (1994) Ethological study of yawning in primates. 1. Quantitative analysis and study of causation in 2 species of Old World monkeys (Cercocebus albigena and Macaca fascicularis). Ethology, 98, 221–245.

di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: A neurophysiological study. Experimental Brain Research, 91, 176–180.

Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119, 593–609.

Gallese, V., Keysers, C., & Rizzolati, G. (2004). A unifying view of the basis of social cognition. Cognitive Sciences, 8(9), 396-403.

Gallup, A. C., Miller, M. L. & Clark, A. B. (2009). Yawning and thermoregulation in budgerigars, Melopsittacus undulates. Animal Behaviour, 77, 109e113.

Harr, A.L., Gilbert, V.R. & Phillips, K.A. (2008). Do dogs (Canis familiaris) show contagious yawning? Animal Cognition, 12, 833-837.

Hickok, G. (2008). Eight Problems for the Mirror Neuron Theory of Action Understanding in Monkeys and Humans. Journal of Cognitive Neuroscience, 27(7), 1229-1243.

Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J.C., & Rizzolatti, G. (2005). Grasping the Intentions of Others with One's Own Mirror Neuron System. PLoS Biology, 3(3), e79. doi:10.1371/journal.pbio.0030079.

Järveläinen, J., Schürmann, M., Avikainen, S., & Hari, R. (2001). Stronger reactivity of the human primary motor cortex during observation of live rather than video motor acts. Neuroreport, 12, 3493-3495.

Joly-Mascheroni R.M., Senju, A., & Shepherd, A.J. et al. (2008). Dogs Catch Human Yawns. Biology Letters, 4, 446-448.

Norscia, I. & Palagi, E. (2011). Yawn Contagion and Empathy in Homo sapiens. PLOS One, 6(12): e28472. doi:10.1371/journal.pone.0028472.

Paukner, A. & Anderson, J. R. (2006). Video-induced yawning in stumptail macaques (Macaca arctoides). Biology Letters 2, 36–38.

Platek, M.S., Critton, S.R., Myers, T.E. & Gallup, G.G. (2003). Contagious yawning: the role of self-awareness and mental state Attribution. Cognitive Brain Research 17, 223–227.

Platek, S.M., Mohamed, F.B., & Gallup, G.G. (2005). Contagious yawning and the brain. Brain Res Cogn Brain Res, 23, 448–452.

Preston, S. D. & de Waal, F. B. (2002). Empathy: Its ultimate and proximate bases. Behav. Brain Sci. 25, 1–20.

Provine, R.R. (1986). Yawning as a Stereotyped Action Pattern and Releasing Stimulus. Ethology, 72(2), 109-122.

Rizzolatti, G., & Craighero, L. (2004). The Mirror-Neuron System. Annu. Rev. Neurosci, 27, 169 92.

Schürmann, M., Hesse, M.D., Stephan, K.E., Saarela, M., Zilles, K., Hari, R., & Fink, G.R. (2005). Yearning to yawn: the neural basis of contagious yawning. Neuroimage, 24, 1260 1264.

Senju, A., Maeda, M., Kikuchi, Y., Hasegawa, T., Tojo, Y. & Osanai, H. (2007). Absence of contagious yawning in children with autism spectrum disorder. Biology Letters 3, 706 708.

No comments: