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Mu Wave Suppression During the Perception of Meaningless Syllables G Model NSY 3299 1–6 ARTICLE IN PRESS Neuropsychologia xxx (2009) xxx–xxx Contents lists available at ScienceDirect Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia 1 Mu wave suppression during the perception of meaningless syllables: 2 EEG evidence of motor recruitment ∗ 3 Stephen Crawcour, Andrew Bowers, Ashley Harkrider, Tim Saltuklaroglu 4 Department of Audiology and Speech Language Pathology, University of Tennessee, 553 S. Stadium Hall, Knoxville, TN 37996-0740, United States 5 6 article info abstract 7 8 Article history: Motor involvement in speech perception has been recently studied using a variety of techniques. In the 9 Received 11 December 2008 current study, EEG measurements from Cz, C3 and C4 electrodes were used to examine the relative power 10 Received in revised form 16 April 2009 of the mu rhythm (i.e., 8–13 Hz) in response to various audio-visual speech and non-speech stimuli, as 11 Accepted 3 May 2009 suppression of these rhythms is considered an index of ‘mirror neuron’ (i.e., motor) activity. Fourteen 12 Available online xxx adult native English speaking females watched and listened to nine audio-video stimuli clips assembled 13 from three different auditory stimuli (speech, noise, and pure tone) combined with three different video 14 Keywords: stimuli (speech, noise, and kaleidoscope—made from scrambling an image from the visual speech). Rel- 15 Mirror neuron 16 Speech perception ative to the noise–noise (baseline condition), all visual speech conditions resulted in significant levels of 17 Electroencephalography suppression, a finding that is consistent with previous reports of mirror activity to visual speech and mu 18 Syllables suppression to ‘biological’ stimuli. None of the non-speech conditions or conditions in which speech was 19 Sensory presented via audition only resulted in any significant suppression of the mu rhythm in this population. Thus, visual speech perception appears to be more closely associated with motor activity than acoustic speech perception. It is postulated that in this study, the processing demands incurred by the task were insufficient for inducing significant mu suppression via acoustic speech only. The findings are discussed in theoretical contexts of speech perception and the mirror system. We suggest that this technique may offer a cost-efficient, non-invasive technique for measuring motor activity during speech perception. © 2009 Published by Elsevier Ltd. 20 1. Introduction they are produced and co-articulated in the vocal tract. It is these 39 gestures that are thought to form the invariants for both perception 40 21 The processes underlying human speech perception have been and production, linking the two processes and allowing them to 41 22 widely examined and debated over the last six decades or so. By operate efficiently and effectively, together as one, in a specialized 42 23 some accounts, speech is perceived as a function of its acoustic con- linguistic manner. As such, under this ‘motor theory’, the dynamic 43 24 stituents and their impact on the auditory system (Klatt, 1979; Kuhl architecture of the mechanism employed to produce speech plays 44 25 & Miller, 1975; Massaro & Cohen, 1990; Ohala, 1996; Stevens, 1981; an essential role in its perception. 45 26 Sussman, 1989). Additionally, these acoustic theories generally hold Conceptually, motor theory appeared to answer many questions 46 27 that speech perception and production are distinct processes. Crit- regarding the nature of speech, yet one of its downfalls was a rel- 47 28 icisms of these perspectives were propagated by studies showing ative dearth of physiological evidence for the neural connectivity 48 29 the lack of acoustic invariance in similar speech percepts (Liberman, between speech perception and production. The discovery of mir- 49 30 Cooper, Shankweiler, & Studdert-Kennedy, 1967), the influence of ror neurons in the ventral premotor cortex (area F5) of the macaque 50 31 visual stimuli on speech percepts (e.g., McGurk effect; McGurk & monkey (Di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992; 51 32 MacDonald, 1976), the phenomenon of categorical perception (e.g., Rizzolatti, Fadiga, Gallese, & Fogassi, 1996) provides compelling 52 33 Mann & Liberman, 1983), and the limited temporal resolution of evidence for motor involvement in sensory processes and there- 53 34 the auditory system for processing rapidly changing acoustic stim- fore, a central linking of perception and production. Neurons in this 54 35 uli (Liberman, 1957; Liberman, Delattre, & Cooper, 1952). As such, motor region, which is considered to be a homolog of Broca’s area 55 36 Liberman and Mattingly (1985) proposed an alternative viewpoint. in humans (Rizzolatti & Craighero, 2004), were found to fire both 56 37 They suggested that speech is perceptually coded as a sequence of when monkeys performed or observed goal directed actions (e.g., 57 38 dynamic ‘gestures’, that are representative of the manner in which grasping). The location and firing patterns of these ‘mirror neurons’ 58 helped support the notion of motor involvement in speech per- 59 ception (Liberman & Whalen, 2000) and theoretical perspectives 60 ∗ of human communication evolving from this observation/action 61 Corresponding author. UNCORRECTED PROOF 62 E-mail address: [email protected] (T. Saltuklaroglu). matching system. This neural matching system is thought to 0028-3932/$ – see front matter © 2009 Published by Elsevier Ltd. doi:10.1016/j.neuropsychologia.2009.05.001 Please cite this article in press as: Crawcour, S., et al. Mu wave suppression during the perception of meaningless syllables: EEG evidence of motor recruitment. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.05.001 G Model NSY 3299 1–6 ARTICLE IN PRESS 2 S. Crawcour et al. / Neuropsychologia xxx (2009) xxx–xxx 63 create a biological link between senders and receivers of gestural degraded (Callan et al., 2003). In addition, it is not clear how brain 129 64 goals, which may have served in the evolution of communication regions involved in speech production are differentially activated 130 65 (Rizzolatti & Arbib, 1998). These notions were further bolstered by during various perception tasks. For example, it has been sug- 131 66 the discovery of a subclass of mirror neurons that fired not only in gested that motor recruitment might be influenced by the degree 132 67 response to seeing an action, but also to hearing sounds associated of linguistic processing necessary to a task (Callan, Jones, Callan, & 133 68 with a specific action such as paper ripping (Kohler et al., 2002) Akahane-Yamada, 2004; Ojanen et al., 2005; Wilson & Iacoboni, 134 69 or peanut breaking (Keysers et al., 2003). Hence, the authors sug- 2006). Thus, the numerous measures of motor recruitment in 135 70 gested that mirror neurons code the intended goal of an action in speech perception and the variety of stimuli employed, combined 136 71 an abstract amodal manner rather than a specific action itself, elic- with the diversity of findings, make it difficult to reconcile the dis- 137 72 iting strong parallels to the nature of speech ‘gestures’ as described crepancies within the current body of research and explain the 138 73 by motor theorists. extent to which motor recruitment may be necessary in speech 139 74 A growing body of research suggests that in humans, the mirror perception. As such, further investigation in this area is warranted. 140 75 system may be involved in action recognition, imitation, empa- Electroencephalography (EEG) has been suggested as a promis- 141 76 thy and theory of mind. Its role in speech perception also has ing, cost-efficient and non-invasive means of indirectly examining 142 77 been scrutinized using various measures. In the auditory modal- the mirror neuron activity in humans. In particular, measurements 143 78 ity, transcranial magnetic stimulation (TMS) has been used to show of oscillation amplitudes in the mu frequencies (8–13 Hz) mea- 144 79 that listening to lingual speech sounds could evoke stronger motor sured across the sensorimotor cortices acquired via surface level 145 80 evoked potentials (MEPs) in the tongue relative to non-speech electrodes are thought to provide a valid index of mirror activ- 146 81 sounds (Fadiga, Craighero, Buccino, & Rizzolatti, 2002) and stronger ity (Altschuler, Vankov, Wang, Ramachandran, & Pineda, 1997). 147 82 MEPs in lip muscles when listening to speech while watching white Mu ‘rhythms’ are influenced by both motor activity and atten- 148 83 noise (Watkins & Paus, 2004; Watkins, Strafella, & Paus, 2003). tion (see Pineda, 2005 for full review). When a person is at rest, 149 84 In addition, using functional magnetic resonance imaging (fMRI), amplitudes of waves in this band are highest because sensorimotor 150 85 listening to meaningless speech has been found to bilaterally acti- neurons responsible for generating these waves fire synchronously. 151 86 vate portions of the ventral premotor cortex (though not Broca’s Conversely, when a person performs an action, the pattern of fir- 152 87 area), portions of the motor cortex, and the supplementary motor ing is asynchronized, resulting in suppression of the mu wave 153 88 area (Wilson, Saygin, Sereno, & Iacoboni, 2004) and motor cortical and smaller amplitudes. However, a number of studies also have 154 89 regions in a somatotopic manner (Pulvermüller et al., 2006) rela- found that mu waves are suppressed when normal adults observe 155 90 tive to non-speech stimuli. In the visual modality, Nishitani and Hari human hand movements (Muthukumaraswamy & Johnson, 2004; 156 91 (2002) used magnetoecepahlography (MEG) to reveal that observ- Muthukumaraswamy, Johnson, & McNair, 2004; Oberman et al., 157 92 ing still pictures of lips could activate Broca’s area and the motor 2005; Virji-Babul et al., 2008) and implied point-light human bio- 158 93 cortex. Similar bilateral motor activation patterns have also been logical animation (Saygin, Wilson, Hagler, Bates, & Sereno, 2004; 159 94 found to silent speech lip movements using fMRI (Campbell et al., Ulloa & Pineda, 2007), and even when participants imagine biolog- 160 95 2001) and stilled speech (Calvert & Campbell, 2003).
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