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MIT HST 722J - Neural mechanisms underlying auditory feedback control of speech

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AbstractIntroductionMethodsVoxel-based analysisStructural equation modelingResultsVoxel-based analysisRegion of interest analysisDiscussionConclusionsAcknowledgmentsReferencesNeural mechanisms underlying auditory feedback control of speech Jason A. Tourville1,*, Kevin J. Reilly1, and Frank H. Guenther1,2,3,4 1Department of Cognitive and Neural Systems Boston University 677 Beacon St. Boston, MA, 02215 Telephone: (617) 353-5765 Fax Number: (617) 353-7755 Email: [email protected] 2Division of Health Sciences and Technology, Harvard University – Massachusetts Institute of Technology 3Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital 4Research Laboratory of Electronics, Massachusetts Institute of Technology *corresponding author Keywords: auditory feedback control, speech production, neural modeling, functional magnetic resonance imaging, structural equation modeling, effective connectivity Abstract The neural substrates underlying auditory feedback control of speech were investigated using a combination of functional magnetic resonance imaging (fMRI) and computational modeling. Neural responses were measured while subjects spoke monosyllabic words under two conditions: (i) normal auditory feedback of their speech, and (ii) auditory feedback in which the first formant frequency of their speech was unexpectedly shifted in real time. Acoustic measurements showed compensation to the shift within approximately 135 ms of onset. Neuroimaging revealed increased activity in bilateral superior temporal cortex during shifted feedback, indicative of neurons coding mismatches between expected and actual auditory signals, as well as right prefrontal and Rolandic cortical activity. Structural equation modeling revealed increased influence of bilateral auditory cortical areas on right frontal areas during shifted speech, indicating that projections from auditory error cells in posterior superior temporal cortex to motor correction cells in right frontal cortex mediate auditory feedback control of speech.1Introduction While many motor acts are aimed at achieving goals in three-dimensional space (e.g., reaching, grasping, throwing, walking, and handwriting), the primary goal of speech is an acoustic signal that transmits a linguistic message via the listener’s auditory system. For spatial tasks, visual feedback of task performance plays an important role in monitoring performance and improving skill level (Redding and Wallace, 2006; Huang and Shadmehr, 2007). Analogously, auditory information plays an important role in monitoring vocal output and achieving verbal fluency (Lane and Tranel, 1971; Cowie and Douglas-Cowie, 1983). Auditory feedback is crucial for on-line correction of speech production (Lane and Tranel, 1971; Xu et al., 2004; Purcell and Munhall, 2006b) and for the development and maintenance of stored motor plans (Cowie and Douglas-Cowie, 1983; Purcell and Munhall, 2006a; Villacorta, 2006). The control of movement is often characterized as involving one or both of two broad classes of control. Under feedback control, task performance is monitored during execution and deviations from the desired performance are corrected according to sensory information. Under feedforward control, task performance is executed from previously learned commands, without reliance on incoming task-related sensory information. Speech production involves both feedforward and feedback control, and auditory feedback has been shown to impact both control processes (Houde and Jordan, 1998; Jones and Munhall, 2005; Bauer et al., 2006; Purcell and Munhall, 2006a). Early evidence of the influence of auditory feedback on speech came from studies showing that speakers modify the intensity of their speech in noisy environments (Lombard, 1911). Artificial disruption of normal auditory feedback in the form of temporally delayed feedback induces disfluent speech (Yates, 1963; Stuart et al., 2002). Recent studies have used transient, unexpected auditory feedback perturbations to demonstrate auditory feedback control of speech. Despite being unable to anticipate the perturbation, speakers respond to pitch (Larson et al., 2000; Donath et al., 2002; Jones and Munhall, 2002; Natke et al., 2003; Xu et al., 2004) and formant shifts (Houde and Jordan, 2002; Purcell and Munhall, 2006b) by altering their vocal output in the direction opposite the shift. These compensatory responses act to steer vocal output closer to the intended auditory target. The ease with which fluent speakers are able to coordinate the rapid movements of multiple articulators, allowing production of as many as 4-7 syllables per second (Tsao and Weismer, 1997), suggests that speech is also guided by a feedforward controller (Neilson and Neilson, 1987). Our ability to speak effectively when noise completely masks auditory feedback (Lane and Tranel, 1971; Pittman and Wiley, 2001) and the maintained intelligibility of post-lingually deafened individuals (Cowie and Douglas-Cowie, 1983; Lane and Webster, 1991) are further evidence of feedforward control mechanisms. The existence of stored feedforward motor commands that are tuned over time by auditory feedback is provided by studies of sensorimotor adaptation (Houde and Jordan, 2002; Jones and Munhall, 2002; Jones and Munhall, 2005; Purcell and Munhall, 2006a). Speakers presented with auditory feedback containing a persistent shift of the formant frequencies (which constitute important cues for speech perception) of their own speech, will adapt to the perturbation by changing the formants of their speech in the direction opposite the shift. Following adaptation, utterances made immediately after removal or masking of the perturbation typically contain formants that differ from baseline formants in the direction opposite the induced perturbation (e.g., Purcell and Munhall, 2006a). These “overshoots” following adaptation indicate a reorganization of the sensory-motor neural mappings that underlie feedforward control in speech (e.g., 1Purcell and Munhall, 2006a) The same studies also illustrate that the feedforward speech controller continuously monitors auditory feedback and is modified when that feedback does not meet expectations. The DIVA model of speech production (Guenther et al., 1998; Guenther et al., 2006) is a quantitatively defined neuroanatomical model that provides a parsimonious account of how auditory feedback is used for both feedback control and for


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