Mirror neuron activity during contagious yawning—an fMRI study

Brain Imaging and Behavior (2013) 7:28–34 DOI 10.1007/s11682-012-9189-9 ORIGINAL RESEARCH Mirror neuron activity during contagious yawning—an fMRI study Helene Haker & Wolfram Kawohl & Uwe Herwig & Wulf Rössler Published online: 7 July 2012 # Springer Science+Business Media, LLC 2012 Abstract Yawning is contagious. However, little research has been done to elucidate the neuronal representation of this phenomenon. Our study objective was to test the hypothesis that the human mirror neuron system (MNS) is activated by visually perceived yawning. We used functional magnetic resonance imaging to assess brain activity during contagious yawning (CY). Signal-dependent changes in blood oxygen levels were compared when subjects viewed videotapes of yawning faces as opposed to faces with a neutral expression. In response to yawning, subjects showed unilateral activation of their Brodmann’s area 9 (BA 9) portion of the right inferior frontal gyrus, a region of the MNS. In this way, two individuals could share physiological and associated emotional states based on perceived motor patterns. This is one component of empathy (motor empathy) that underlies the development of cognitive empathy. The BA 9 is reportedly active in tasks requiring mentalizing abilities. Our results emphasize the connection between the MNS and higher cognitive empathic functions, including mentalizing. We conclude that CY is based on a functional substrate of empathy. Keywords Empathy . fMRI . Mirror neuron system . Social cognition . Imitation . Resonance . Inferior frontal gyrus Abbreviations BA Brodmann’s Area BOLD Blood oxygenation level-dependent CY Contagious yawning fMRI Functional magnetic resonance imaging IFG Inferior frontal gyrus H. Haker (*) : W. Kawohl : U. Herwig : W. Rössler Department of General and Social Psychiatry, Psychiatric University Hospital Zurich, Militärstrasse 8, POB 1930, 8021 Zürich, Switzerland e-mail: IPL MNS STS Inferior parietal lobule Mirror neuron system Sulcus temporalis superior Introduction Little research has been done to elucidate an origin for the fascinating phenomenon of contagious yawning (CY) (Provine 1986). In contrast to spontaneous yawning, which is considered evolutionarily old (Vischer 1959; Sepulveda and Mangiamarchi 1995), CY is phylogenetically and ontogenetically young, and may not appear until the second year after birth (Piaget 1951; Provine 1989; Anderson and Meno 2003). Whereas CY occurs in only a limited number of animal species besides humans, including chimpanzees (Anderson et al. 2004), macaques (Paukner and Anderson 2006), baboons (Palagi et al. 2009), and dogs (Joly-Mascheroni et al. 2008), spontaneous yawning can be found in almost all vertebrates. Why does CY require such a high degree of evolutionary and developmental specialization? CY is an interaction between two individuals, with one person experiencing and sharing the physiological and emotional state of the other, and a mechanism for synchronizing the state of a group. This implicit link between two persons in CY is considered an easily observable sign of empathy (Lehmann 1979; Provine 2005; Senju 2010; Arnott et al. 2009). CY is impaired in children with autism spectrum disorder (Senju et al. 2007; Senju et al. 2009), patients with PTSD (Nietlisbach et al. 2010), and those with schizophrenia (Haker and Rössler 2009) or schizotypal personality traits (Platek et al. 2003). All of these conditions are accompanied by reduced empathic abilities. Currently accepted concepts of empathy state that contagion constitutes one functional component of empathy—motor empathy—and is mediated by brain areas involved in the mirror neuron system (MNS) Brain Imaging and Behavior (2013) 7:28–34 (Gallese 2007; Preston and de Waal 2002; Leslie et al. 2004; Blair 2005; Decety and Lamm 2006; Keysers and Gazzola 2007; Uddin et al. 2007; Haker et al. 2010) The MNS is a network of visuo-motor neurons that was first discovered in a macaque in area F5 of the pre-motor cortex (Rizzolatti et al. 1996). These neurons are active when a particular action is performed or when the same action, done by another individual, is observed. Mirror neurons with similar properties have been found in the posterior parietal cortex, reciprocally connected with area F5 (Rizzolatti et al. 2001). Experimental evidence suggests that an analogous action observation–execution matching system exists in humans. Studies using electroencephalography, trans-cranial magnetic stimulation, positron emission tomography, and functional magnetic resonance imaging (fMRI) have revealed a network composed of the pars opercularis of the inferior frontal gyrus (IFG), the anterior part of the inferior parietal lobule (IPL), and the superior temporal sulcus (STS) (Rizzolatti and Sinigaglia 2010). Because one’s own motor patterns can be activated while observing an individual and anticipating its effect from the same perspective as the one who is acting, the mirror mechanism generates the basis for shared perception (Gallese 2003). In this way not only simple motor actions but also emotional states can be shared, as if by contagion, between human beings (Carr et al. 2003). By applying video sequences, Platek et al. (2005) have found bilateral activity in the posterior cingulate and in the precuneus of individuals exposed to yawning faces contrasted to laughing faces. These regions belong to a medial fronto-parietal network that mediates processes focused on internal, mental, emotional, and experiential characteristics of others or oneself (Lieberman 2006). Schürmann et al. (2005) have reported that the right STS is activated when a person is stimulated by a video-taped yawning face but not one that is performing similar non-yawning mouth movements. The STS is a region of the externally oriented fronto-parietal network, which is thought to represent the main visual input to the MNS and to detect specifically socially meaningful stimuli (Iacoboni 2005). Our aim was to search for possible activation of regions associated with the MNS, as IFG (as a motor core of the human MNS), as well as the IPL and STS (Rizzolatti and Craighero 2004), during visual contagion by yawning. This mechanism, as hypothesized by Cooper et al. (2008), has been found in auditory contagious yawning by Arnott et al. (2009) but, according to our knowledge, has not yet been verified in a visual paradigm. To compare the effects of stimulations, we used video sequences that depicted yawning faces in contrast to faces showing minimal, physiological, smooth-head, -mouth, and -gaze movements by a person scanning the environment without emotional mimic expression (i.e., a non- 29 contagious biological motion). We conducted fMRI to monitor changes in blood oxygen level-dependent (BOLD) signals. In contrast to the above-mentioned study by Platek et al. (2005), who contrasted a neutral condition against two contagious conditions, yawning and laughing, we considered our contrast to be (...truncated)