Differential cerebral activation during observation of expressive gestures and motor acts

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Abstract

We compared brain activation involved in the observation of isolated right hand movements (e.g. twisting a lid), body-referred movements (e.g. brushing teeth) and expressive gestures (e.g. threatening) in 20 healthy subjects by using functional magnetic resonance imaging (fMRI). Perception-related areas in the occipital and inferior temporal lobe but also the mirror neuron system in the lateral frontal (ventral premotor cortex and BA 44) and superior parietal lobe were active during all three conditions. Observation of body-referred compared to common hand actions induced increased activity in the bilateral posterior superior temporal sulcus (STS), the left temporo-parietal lobe and left BA 45. Expressive gestures involved additional areas related to social perception (bilateral STS, temporal poles, medial prefrontal lobe), emotional processing (bilateral amygdala, bilateral ventrolateral prefrontal cortex (VLPFC), speech and language processing (Broca's and Wernicke's areas) and the pre-supplementary motor area (pre-SMA). In comparison to body-referred actions, expressive gestures evoked additional activity only in the left VLPFC (BA 47). The valence-ratings for expressive gestures correlated significantly with activation intensity in the VLPFC during expressive gesture observation. Valence-ratings for negative expressive gestures correlated with right STS-activity. Our data suggest that both, the VLPFC and the STS are coding for differential emotional valence during the observation of expressive gestures.

Introduction

Several studies in monkeys, descriptions of deficits of patients with circumscribed lesions and functional imaging studies have been performed on the topic of gesture observation and recognition. These studies demonstrated that differential brain areas are active during observation of specific aspects of meaningful gestures. However, different types of hand gestures within the same pool of subjects were so far not assessed. On the basis of previous studies we selected three types of meaningful gestures: isolated hand movements, body-referred hand movements and expressive gestures performed with one hand. In order to compare cerebral activation during the observation of these three gesture types we used functional magnetic resonance imaging (fMRI) during gesture observation in 20 healthy subjects.

The perception of gestures in contrast to other objects presented is distinct already at the level of the occipito-temporal junction (Peigneux et al., 2000). In monkeys, Mishkin and Ungerleider (1982) differentiated a ventral pathway, related to object recognition (face and form; via V3 and inferior parietal), and a dorsal pathway for visual guidance of actions towards objects (movement; via V5 and superior parietal). During observation of hand actions monkeys show increased activation in the dorsal pathway (Fadiga, Fogassi, Pavesi, & Rizzolatti, 1995). Neurons mirroring hand movements are located in F5 (“mirror neurons”: di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992; Rizzolatti & Arbib, 1998; Rizzolatti, Fadiga, Gallese, & Fogassi, 1996). The human homologue to F5 is probably BA 44 within the pars opercularis of the inferior frontal gyrus (Rizzolatti, Fogassi, & Gallese, 2002) overlapping with the ventral premotor cortex (PMC; lateral BA 6). Patients with lesions in BA 44 and BA 6 failed to show deficits in movement imitation and observation (Haaland, Harrington, & Knight, 2000)—probably because this ability is represented bilaterally (Muhlau et al., 2005). Although the pars opercularis of the left inferior frontal gyrus and the adjacent premotor cortex are predominantly active during imitation of movements (Buccino et al., 2004; Grezes, Armony, Rowe, & Passingham, 2003; Heiser, Iacoboni, Maeda, Marcus, & Mazziotta, 2003; Iacoboni et al., 1999) and especially during target-directed movements (Koski et al., 2003), this area is also active during observation of hand (Binkofski et al., 1999a, Binkofski et al., 1999b; Nishitani & Hari, 2000) and body movements (Buccino et al., 2001). Additional areas related to language production and perception – such as Broca's and Wernicke's area – have been demonstrated to be active if meaningful common hand movements were compared with meaningless ones (Decety et al., 1997).

Mirror neurons might not be restricted to the frontal lobe since they have also been described in the inferior parietal gyrus (Fogassi et al., 2005; Rizzolatti, Fogassi, & Gallese, 2001). These mirror neurons inferior to the parietal sulcus might allow the monkey to understand the intentions of the actor of the observed movements.

Humans with parietal lesions often present symptoms of apraxia. Ideational and ideomotor apraxias represent supramodal apraxias, i.e. the disturbed motor behavior is not restricted to a particular modality but affects the ideation, and conception of the intended motor acts at a global level. These most complex forms of apraxia have been associated with lesions of the supramarginal or angular gyrus (Freund, 1992).

During movement imitation these patients show predominantly deficits for body-referred hand movements but less for isolated hand gestures (Goldenberg, 1995, Halsband et al., 2001).

Original models of apraxia have already described that these patients display not only production deficits but also deficits in gesture perception (Roy & Square, 1985) and other studies support this opinion (Goldenberg, 1999).

Both, the dorsal pathway and ventral pathway terminate in a common polysensory area, the superior temporal sulcus (STS), where the perception of form and motion interact (Oram & Perrett, 1996; Vaina, Solomon, Chowdhury, Sinha, & Belliveau, 2001). This area might be responsible for the matching of an observed movement with a stored motor representation (Iacoboni et al., 2001). In the STS, both facial and hand movements are analyzed according to their social significance (Allison, Puce, & McCarthy, 2000). The STS is part of the so-called “theory of mind” areas (Frith & Frith, 1999), additionally consisting of the dorsal PMC and the temporal poles (Gallagher & Frith, 2003; Vogeley et al., 2001) and is active during setting oneself into another's perspective (“mentalizing”). It has been shown that these areas are involved in the perception of expressive gestures (Gallagher & Frith, 2004).

In comparison to body-referred movements expressive gestures are usually associated with emotional responses predominantly expressed via facial characteristics. The medial part of the ventral PFC is involved in the active analysis and evaluation of the emotional valence of pictures and facial expressions (e.g. Phan et al., 2004). In contrast, the VLPFC might be more associated with the passive perception of emotional stimuli (facial expressions: Blair, Morris, Frith, Perrett, & Dolan, 1999; perception of emotional intonation: Wildgruber et al., 2004). This area has recently been described as an area important for the feelings of sadness after the presentation of sad films in adults (Levesque et al., 2003) and children (Levesque et al., 2004). Additionally, expressive gestures are not only used for emotional interaction but also for neutral information which carry a semantic content. In contrast to body-referred movements this content is performed to interact with another subject and its semantic component has to be decoded—comparable to sign language recognition (Goldin-Meadow, 1999).

We hypothesized that observation of all three type of movements (isolated hand movements, body-referred movements and expressive gestures) might be associated with activation in the ventral and the dorsal pathway including the frontal and parietal “mirror neurons”.

The inferior parietal lobe was expected to be more involved during observation of body-referred movements than of isolated hand movements, since patients with lesions in this area show higher deficits in imitation of body-referred compared to isolated hand movements. The involvement of the STS should be increased when more socially relevant objects are observed. Therefore, body-referred movements should elicit more STS-activation than isolated hand movements. Additionally, we hypothesized that activation of Broca's and Wernicke's areas might be enhanced during observation of expressive gestures being highly communicative in its purpose. Finally, we hypothesized that the increasing emotional content of expressive gestures might result in increased activation of areas processing emotions. In a correlation analysis we tested the possible correlation of valence ratings of the expressive gestures with BOLD effect magnitude in regions of interest. Most reasonable candidates would be the amygdala, important for facial expression observation (Blair et al., 1999, Breiter et al., 1996; Hariri et al., 2000; Iidaka et al., 2001), the VLPFC and the adjacent pars opercularis of the inferior frontal gyrus which has been shown to be involved in passive perception of emotional stimuli in different modalities and the STS which is highly important for processing of social relevant stimuli.

Section snippets

Subjects

Twenty volunteers (mean age 52.30 years; S.D. = 12.40; range: 22–69 years; 10 male) without history of neurological or psychiatric disease were recruited by announcements at the University and a local adult education center. All participants were right handed (lateralization quotient for the right side of more than 90%) as assessed by the Edinburgh Handedness Inventory (Oldfield, 1971). The study was approved by the Ethics Committee of the Medical Faculty of the University of Tübingen. Written

Rating of video-clips

The participants did not differ in the recognition of presented gestures (average of number of errors 2.65; Mann–Whitney U-test: z = 1.81; n.s.) and the emotional valence of expressive gestures (negative average: −3.23; positive average: 2.37; n.s.; range: −5 to 5) in comparison to the reference group.

fMRI-effects for all stimuli

All types of gestures induced activation in the bilateral occipito-temporal junction including V3, V5 and face recognition areas in the inferior temporal lobe (fusiform gyrus; see Supplementary

Discussion

In this study we investigated all three types of gestures (isolated hand movements, body-referred movements and expressive gestures) in the same group of healthy subjects. Comparison between activation maps obtained during observation of isolated hand movements, body-referred movements and expressive gestures revealed differences between these types of gestures. Differences emerged especially in areas associated with social perception and emotional valence.

Conclusion

We observed different activation sites, which have been described to be involved in emotional and semantic processing, mentalizing and object recognition during the observation of different types of meaningful gestures. Our data point to the importance of the parieto-temporal cortex for the observation of body-referred motor acts. Furthermore, they highlight the importance of areas involved in social interaction and the VLPFC for expressive gesture recognition.

Acknowledgements

We thank Martin Kircher for help with the computerized video presentation in the scanner. The study was supported by the “Deutsche Forschungsgemeinschaft”. N.B. is also supported by the National Institutes of Health.

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