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Modulation of Motor Excitability During Speech Perception: the Role of Broca’S Area

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Modulation of Motor Excitability During Speech Perception: the Role of Broca’S Area Modulation of Motor Excitability during Speech Perception: The Role of Broca’s Area Kate Watkins and Toma´ˇs Paus Abstract & Studies in both human and nonhuman primates indicate regions that modulate the excitability of the motor system that motor and premotor cortical regions participate in during speech perception. Our results show that during auditory and visual perception of actions. Previous studies, auditory speech perception, there is increased excitability of using transcranial magnetic stimulation (TMS), showed that motor system underlying speech production and that this perceiving visual and auditory speech increased the excitability increase is significantly correlated with activity in the posterior of the orofacial motor system during speech perception. Such part of the left inferior frontal gyrus (Broca’s area). We propose studies, however, cannot tell us which brain regions mediate that this area ‘‘primes’’ the motor system in response to heard this effect. In this study, we used the technique of combining speech even when no speech output is required and, as such, positron emission tomography with TMS to identify the brain operates at the interface of perception and action. & INTRODUCTION perceptions to phonetic gestures and that such a system The division between the brain regions involved in might be at the origin of the evolution of human speech action production and perception is becoming increas- (Rizzolatti & Arbib, 1998; Gallese et al., 1996). ingly blurred as evidence accumulates that in the In humans, transcranial magnetic stimulation (TMS) primate brain, motor and premotor regions also par- applied over the primary motor cortex has been used ticipate in action perception. In the domain of speech to probe its excitability during visual perception of perception this notion is not new. In fact, Liberman actions (Aziz-Zadeh, Maeda, Zaidel, Mazziotta, & Iacobo- and Mattingly (1985), in their motor theory of speech ni, 2002; Gangitano, Mottaghy, & Pascual-Leone, 2001; perception, first raised the possibility that perception Strafella & Paus, 2000; Fadiga, Fogassi, Pavesi, & Rizzo- of speech involves access to the speech production latti, 1995). In such studies, motor-evoked potentials are system. elicited in a target muscle by stimulating the appropriate In the monkey, a number of studies have identified region of the primary motor cortex. During perception neurons in the ventral premotor cortex that are active of actions that involve the target muscle, motor-evoked during production of actions and visual perception of potentials increase in size, indicating that the motor the same actions (Gallese, Fadiga, Fogassi, & Rizzolatti, system underlying production of the perceived action 1996; DiPellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, is in a state of increased excitability, or lowered thresh- 1992). These ‘‘mirror neurons’’ may play a role, there- old. Electro- and magnetoencephalography during visual fore, in the recognition, understanding, and imitation of perception of hand movements also reveal changes in actions (Umilta et al., 2001; Rizzolatti, Fadiga, Fogassi, & the primary motor cortex, which are similar to those Gallese, 1999). Recently, neurons in the ventral premo- seen during movement execution (Cochin, Barthelemy, tor cortex of the monkey were found to be active not Roux, & Martineau, 1999; Hari et al., 1998). only when the monkey sees another individual execut- In the speech domain, several studies using methods ing an action but also when it hears the sound associ- similar to those described earlier have examined motor ated with the action (e.g., the sound of paper tearing or cortex changes during visual and auditory perception of a stick dropping; Kohler et al., 2002). These results (Watkins, Strafella, & Paus, 2003; Fadiga, Craighero, indicate that the premotor cortex participates not only Buccino, & Rizzolatti, 2002; Nishitani & Hari, 2002; in visual but also in auditory perception of actions. Sundara, Namasivayam, & Chen, 2001). In one such Furthermore, it has been proposed that a similar system study, we applied TMS over the face area of the primary exists in the human allowing the matching of phonetic motor cortex to elicit a motor-evoked potential in the orbicularis oris muscle of the lips (Watkins et al., 2003). The size of the motor-evoked potential increased during Montreal Neurological Institute, McGill University both auditory and visual speech perception compared to D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:6, pp. 978–987 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929041502616 by guest on 27 September 2021 control conditions. This increase in motor excitability tentials recorded from the lip muscles (see Figure 1 and during speech perception was only evident for stimula- Methods for further details). tion over the left hemisphere and not for stimulation over the right hemisphere; this pattern is consistent with the RESULTS known specialization of the left hemisphere for speech. In a control experiment, we demonstrated that the size of Eight subjects were scanned using PET. In each subject, the motor-evoked potentials elicited in a muscle of the three scans were obtained for each of the four condi- right hand did not differ among these conditions, sug- tions, with the exception of one subject in whom one gesting that speech-perception-related changes in excit- Speech scan was rejected because the coil moved. ability are specific to the muscles involved in speech Twenty pulses of TMS were applied during each scan. production. In a similar study, Fadiga et al. (2002) showed Motor-evoked potentials were recorded in response to increased motor-evoked potentials recorded from the the TMS pulses using continuous electromyography. tongue when subjects listened to speech sounds that The average sizes of motor-evoked potentials, elicited require movement of the tongue in their production. by TMS, and recorded from the orbicularis oris muscle in The aforementioned TMS studies demonstrate that the Speech, Lips, and Eyes conditions were expressed as perception influences the state of the motor system percentages of those recorded in the Control condition. involved in production. These studies, however, cannot Within-subjects analysis of variance revealed a significant identify the brain region or regions that mediate such effect of condition, F(2,14) = 9.31, p = .003, which was changes in the motor system. In the present study, we due to significantly greater motor-evoked potentials for combined TMS with positron emission tomography the Speech condition relative to the Eyes, t(7) = 5.02, (PET) to identify the brain regions mediating the p = .005, and to the lips, t(7) = 3.55, p = .028 con- changes in motor excitability during perception of ditions (see Figure 2). The two visual conditions did not speech. On the basis of findings in monkey premotor differ significantly. These results confirm that listening to cortex and the homology between this region and the speech increases the excitability of the motor system posterior part of the human inferior frontal gyrus, underlying speech production. In this study, no signifi- known as Broca’s area, we hypothesized that the latter cant change in motor excitability was seen during visual would be one region involved in the modulation of perception of speech-related lip movements. motor excitability during speech perception. Comparison of the PET scans obtained in the Speech, We applied TMS over the face area of the left primary Lips, and Eyes conditions with those obtained in the motor cortex to measure motor excitability during (1) control condition revealed, respectively, the brain regions listening to speech (Speech condition), (2) viewing of involved in listening to speech, viewing speech-related speech-related lip movements (Lips condition), (3) view- lip movements or viewing eye-and-brow movements. ing of eye and brow movements (Eyes condition), and As expected, listening to speech was associated with (4) listening to and viewing noise (Control condition). At strong activation of the superior temporal gyrus bilater- the same time, we scanned the brain using PET to ally, which extended along its length to the uncus in identify regions in which changes in activity, as indexed the anterior temporal lobe (see Figure 3 and Table 1). by cerebral blood flow, correlated with changes in Viewing movements of the face, either lip or eye-and- excitability, measured by the size of motor-evoked po- brow movements, was associated with activation in the Figure 1. Experimental design. Schematic shows examples of the visual and auditory stimuli used in each of the four conditions. PET data were acquired over 60 sec during the application of 20 magnetic pulses to the primary motor cortex face area. Watkins and Paus 979 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929041502616 by guest on 27 September 2021 whether the slope of the regression line at each voxel was significantly different from zero. For the Speech conditions, significant positive correlations were seen in the opercular region of the left inferior frontal gyrus (area 44/45), the left putamen, a very medial portion of the left parietal operculum, and the left cerebellum (lobules IV, V, and VI) (Table 2 and Figure 4). Significant negative correlations were seen in the left supramarginal gyrus (in a very lateral portion of the parietal opercu- lum) and the area of the right precentral gyrus that corresponds
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