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.
Introduction
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.
