mise à jour du
28 octobre 2006
J. Neurosci
Positive emotions preferentially engage
an auditory&endash;motor "Mirror" system
Jane E. Warren, Disa A. Sauter, Frank Eisner, Jade Wiland,
M. Alexander Dresner, Richard J. S. Wise,
Stuart Rosen, Sophie K. Scott


Abstract : Social interaction relies on the ability to react to communication signals. Although cortical sensory-motor "mirror" networks are thought to play a key role in visual aspects of primate communication, evidence for a similar generic role for auditorymotor interaction in primate nonverbal communication is lacking. We demonstrate that a network of human premotor cortical regions activated during facial movement is also involved in auditory processing of affective non-verbal vocalizations. Within this auditory-motor "mirror" network, distinct functional subsystems respond preferentially to emotional valence and arousal properties of heard vocalizations.
Positive emotional valence enhanced activation in a left posterior inferior frontal region involved in representation of prototypic actions, while increasing arousal enhanced activation in pre-supplementary motor area cortex involved in higher-order motor control. Our findings demonstrate that listening to non-verbal vocalisations can automatically engage preparation of responsive orofacial gestures, an effect that is greatest for positive-valence and high-arousal emotions.
The automatic engagement of responsive orofacial gestures by emotional vocalizations suggests that auditory-motor interactions provide a fundamental mechanism for mirroring the emotional states of others during primate social behavior. Motor facilitation by positive vocal emotions suggests a basic neural mechanism for establishing cohesive bonds within primate social groups.
The ability to generate appropriate behavioral responses to visual and auditory communication signals is fundamental to social intercourse in many animal species. Increasing evidence suggests that perceptual-motor interaction plays a key role in visual aspects of primate social behavior (Preston and de Waal, 2003; Adolphs, 2003).
In non-human primates, so-called visuo-motor mirror neurons, neurons that discharge during the observation or execution of a particular movement (Gallese et al., 1996), have been implicated in the processing of communicative gestures (Ferrari et al., 2003). Although human visuo-motor mirror responses have been demonstrated from neuronal recordings only rarely (Krolak-Salmon et al., 2006), functional neuroimaging studies have demonstrated cortical-level "mirror" responses to the observation and generation of facial expressions of emotion (Carr et al., 2003; Leslie et al., 2004; Hennenlotter et al., 2005).
In the auditory domain, auditory-motor mirror neurons, responsive to observing an action and hearing the sound of the same action, have been identified in non-human primates (Kohler et al., 2002; Keysers et al., 2003), and there is evidence of interplay between auditory and motor systems within the specialized domain of human speech processing (Fadiga et al., 2002; Watkins et al., 2003; Watkins and Paus, 2004; Wilson et al., 2004), including the processing of affective prosody (Hietanen et al., 1998). However, a generic role for auditory-motor interaction in the communication of non-verbal information, such as emotion, is yet to be established in primates.
In this functional magnetic resonance imaging (fMRI) study, we investigated cortical regions responsive to both the perception of human vocalizations and the voluntary generation of facial expressions. In four auditory-perceptual conditions, subjects listened passively, without overt motor response, to non-verbal emotional vocalizations conveying two positive-valence emotions, amusement and triumph, and two negative-valence emotions, fear and disgust (Ekman, 1992; Ekman, 2003). Use of non-verbal, rather than verbal, vocalizations optimized recognizability of emotional content (Scott et al., 1997) and avoided confounds of phonological and verbal content (Hietanen et al., 1998; Fadiga et al., 2002; Watkins et al., 2003; Hauk et al., 2004; Watkins and Paus, 2004; Wilson et al., 2004).
In a facial movement condition, subjects performed voluntary smiling movements, in the absence of auditory input. We hypothesized that cortical regions showing combined auditory-perceptual and motor responses would be located within premotor and motor cortical regions.
Furthermore, as emotional valence and arousal are widely considered to be critical factors in models of the processing and representation of emotional signals (Russell, 1980), we investigated the effect of these stimulus properties on hemodynamic responses within cortical regions demonstrating auditory-motor "mirror" responses.
Discussion :
This fMRI study demonstrates that passive perception of non-verbal emotional vocalizations automatically modulates neural activity in a network of premotor cortical regions involved in the control of facial movement. Moreover, the degree of activation of specific regions within these premotor regions is determined by emotional valence and arousal properties of affective vocal stimuli. The complementary EMG data clearly demonstrate that these premotor cortical responses do not simply reflect the generation of overt facial movements in response to emotional vocalizations: thus our findings suggest that listening vocal expressions of positive or arousing emotions automatically engages preparation for responsive orofacial gestures.
Our results demonstrate the existence of distinct functional subsystems within this auditory-motor "mirror" network that correspond broadly to known function- and connectivity-based divisions within the primate premotor cortex (Rizzolatti and Luppino, 2001). Premotor responses associated with positive emotional valence were identified at the posterior border of the left IFG. Posterior IFG is the putative human homologue of the non-human primate mirror neuron area F5 (Rizzolatti and Arbib, 1998). In addition to neurons responsive to visual perception of hand and orofacial actions (Gallese et al., 1996), including communicative orofacial gestures (Ferrari et al., 2003), a proportion of area F5 neurons also respond when hearing action-related sounds (Kohler et al., 2002; Keysers et al., 2003). Neurons in primate area F5 are thought to encode motor prototypes; representations of potential actions congruent with a particular stimulus, that can be activated either exogenously via sensory projections, or endogenously (Rizzolatti and Luppino, 2001).
The positive emotions investigated in this study, amusement and triumph, are typically encountered in group situations characterized by mutual and interactive expressions of emotion. Autistic children demonstrate reduced activation in posterior IFG during observation and imitation of emotional facial expressions that correlates with measures of social dysfunction (Dapretto et al., 2006). Our findings suggest that vocal communications conveying positive emotions automatically activate motor representations encoded in posterior IFG, corresponding to a repertoire of orofacial gestures potentially appropriate to the emotional content of the perceived vocal stimulus. This process of auditory-motor interaction may be supported by the primate dorsal auditory pathway (Scott and Johnsrude, 2003; Hickok and Poeppel, 2004; Warren et al., 2005), which includes projections from posterior temporal auditory association cortex to posterior inferior frontal cortex (Deacon, 1992).
Listening to emotionally arousing vocal stimuli was associated with activation in pre- SMA. Depth electrode recordings from human pre-SMA have demonstrated mirrorlike responses when viewing emotional faces (Krolak-Salmon et al., 2006). Pre-SMA corresponds to area F6 in non-human primates, which receives projections fromprefrontal and cingulate cortex (Luppino et al., 1993), and has been implicated in the gating and overall control of visuo-motor transformations on the basis of external contingencies and motivations (Rizzolatti and Luppino, 2001). Highly arousing emotional vocalizations therefore engage a region involved in higher-order aspects of complex motor control. Convergent valence- and arousal-related perceptual responses within the somatotopically-arranged left and right lateral premotor and motor cortices (Buccino et al., 2001; Alkhadi et al, 2002) were maximal in the face motor area (Buccino et al., 2001; Carr et al., 2003; Leslie et al., 2004), but also extended into more ventral regions involved in the motor control of articulation (Murphy et al., 1997; Blank et al., 2002; Wilson et al., 2004).
Lateral premotor activation was found to extend posteriorly into primary motor regions in both hemispheres. Activation of primary motor cortex is typically associated with overt movement, however our EMG study clearly demonstrated that listening to affective vocal stimuli does not elicit overt facial movements or vocalizations. In fact, our results are in keeping with previous fMRI and TMS studies of motor responses during speech perception (Watkins et al, 2003; Wilson et al., 2004) and observation of facial expressions (Carr et al., 2003; Leslie et al, 2004), which have demonstrated that perception of orofacial actions alone is sufficient to increase activity in primary motor cortex.
Due to temporal constraints on fMRI data acquisition, we were unable to incorporate an additional motor condition involving a negative facial expression, such as frowning. Thus, our delineation of cortical regions involved in the generation of facial expressions based solely on a single positive facial expression. It is doubtful, however, that the spatial resolution of fMRI would have been sufficient to demonstrate significant topographical differences in activation for different facial expressions in motor and premotor cortical regions. Moreover, the EMG study failed to demonstrate any significant increase in brow muscle activity during perception of negative-emotion vocalizations. Therefore we would argue that the absence of a motor condition involving a negative facial expression does not compromise the validity of our results.
Taken together, our findings suggest that listeners' motor responses to emotional vocalizations involved more than direct imitative activation of representations of facial or vocal expressions. The recruitment of "mirror" regions during action perception has been attributed not only to unconscious imitation and action recognition (Gallese et al., 1996; Rizzolatti and Arbib, 1998; Rizzolatti and Luppino, 2001; Kohler et al., 2002; Ferrari et al., 2003; Keysers et al., 2003), but also to more complex functions such as understanding the intention or goal of a perceived action (Ferrari et al., 2005; Iacoboni et al., 2005) or the preparation of non-imitative motor responses (Leslie et al., 2004).
Based on our findings, we speculate that listening to vocal expressions of positive or highly arousing emotions activates representations of vocal and facial gestures appropriate to the emotion being communicated. The mirroring of social cues, a process not limited to imitation, is strongly associated with positive valence; for example, mirroring of body posture, gestures and intonation is linked to enhanced establishment of rapport (Chartrand and Bargh, 1999). The greater propensity for positive-valence communications to automatically activate motor representations may be a crucial component in the formation of empathic responses.
We are all familiar with the experience of responding to laughter or cheering with an involuntary smile or laugh. On the basis of this study, we argue that this impulse to respond to affective vocal communications with appropriate orofacial gestures is mediated by the automatic activation of orofacial motor cortical fields. We suggest that the enhanced motor response to perception of positive emotions provides a mechanism for mirroring the positive emotional states of others during primate social interaction. Mirroring behavior improves ease of social interaction (Chartrand and Bargh, 1999): motor facilitation in response to vocal communication of positive emotions may therefore provide a fundamental mechanism for establishing cohesive bonds between individuals in primate social groups. Given the importance of individual bonds and group cohesion for survival in many social species, such a mechanism may not be restricted to primates.