Modulation of Speech Motor Learning with Transcranial Direct Current Stimulation of the Inferior Parietal Lobe

The inferior parietal lobe (IPL) is a region of the cortex believed to participate in speech motor learning. In this study, we investigated whether transcranial direct current stimulation (tDCS) of the IPL could influence the extent to which healthy adults (1) adapted to a sensory alteration of their own auditory feedback, and (2) changed their perceptual representation. Seventy subjects completed three tasks: a baseline perceptual task that located the phonetic boundary between the vowels /e/ and /a/; a sensorimotor adaptation task in which subjects produced the word “head” under conditions of altered or unaltered feedback; and a post-adaptation perceptual task identical to the first. Subjects were allocated to four groups which differed in current polarity and feedback manipulation. Subjects who received anodal tDCS to their IPL (i.e., presumably increasing cortical excitability) lowered their first formant frequency (F1) by 10% in opposition to the upward shift in F1 in their auditory feedback. Subjects who received the same stimulation with unaltered feedback did not change their production. Subjects who received cathodal tDCS to their IPL (i.e., presumably decreasing cortical excitability) showed a 5% adaptation to the F1 alteration similar to subjects who received sham tDCS. A subset of subjects returned a few days later to reiterate the same protocol but without tDCS, enabling assessment of any facilitatory effects of the previous tDCS. All subjects exhibited a 5% adaptation effect. In addition, across all subjects and for the two recording sessions, the phonetic boundary was shifted toward the vowel /e/ being repeated, consistently with the selective adaptation effect, but a correlation between perception and production suggested that anodal tDCS had enhanced this perceptual shift. In conclusion, we successfully demonstrated that anodal tDCS could (1) enhance the motor adaptation to a sensory alteration, and (2) potentially affect the perceptual representation of those sounds, but we failed to demonstrate the reverse effect with the cathodal configuration. Overall, tDCS of the left IPL can be used to enhance speech performance but only under conditions in which new or adaptive learning is required.

[1]  Dottie M. Clower,et al.  The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum , 2001, The Journal of Neuroscience.

[2]  Walter Paulus,et al.  Diminution of training-induced transient motor cortex plasticity by weak transcranial direct current stimulation in the human , 2000, Neuroscience Letters.

[3]  F. Fregni,et al.  Transcranial direct current stimulation for major depression: an updated systematic review and meta-analysis. , 2014, The international journal of neuropsychopharmacology.

[4]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[5]  Josef P. Rauschecker,et al.  An expanded role for the dorsal auditory pathway in sensorimotor control and integration , 2011, Hearing Research.

[6]  V. Gracco,et al.  Auditory-Motor Learning during Speech Production in 9-11-Year-Old Children , 2010, PloS one.

[7]  Daniel R. Lametti,et al.  Sensory Preference in Speech Production Revealed by Simultaneous Alteration of Auditory and Somatosensory Feedback , 2012, The Journal of Neuroscience.

[8]  J. Mattingley,et al.  Is the mirror neuron system involved in imitation? A short review and meta-analysis , 2009, Neuroscience & Biobehavioral Reviews.

[9]  A M Liberman,et al.  Perception of the speech code. , 1967, Psychological review.

[10]  Hideki Kawahara,et al.  Hearing voice: transformed auditory feedback effects on voice pitch control , 1998 .

[11]  H. Diener,et al.  Modulation of human trigeminal and extracranial nociceptive processing by transcranial direct current stimulation of the motor cortex , 2011, Cephalalgia : an international journal of headache.

[12]  Gottfried Schlaug,et al.  Transcranial direct current stimulation in stroke recovery. , 2008, Archives of neurology.

[13]  D. Ostry,et al.  Stimulation of the Posterior Parietal Cortex Interferes with Arm Trajectory Adjustments during the Learning of New Dynamics , 2004, The Journal of Neuroscience.

[14]  C. Bellone,et al.  ON A ROLE , 1996 .

[15]  Felix Wichmann,et al.  The psychometric function: II. Bootstrap-based confidence intervals and sampling , 2001, Perception & psychophysics.

[16]  Vincent L. Gracco,et al.  On the role of the supramarginal gyrus in phonological processing and verbal working memory: Evidence from rTMS studies , 2014, Neuropsychologia.

[17]  Kevin G Munhall,et al.  Adaptive control of vowel formant frequency: evidence from real-time formant manipulation. , 2006, The Journal of the Acoustical Society of America.

[18]  Anjan Chatterjee,et al.  Rethinking the thinking cap , 2011, Neurology.

[19]  Maneesh C. Patel,et al.  Perceptual Systems Controlling Speech Production , 2008, The Journal of Neuroscience.

[20]  J. Perkell,et al.  Sensorimotor adaptation to feedback perturbations of vowel acoustics and its relation to perception. , 2007, The Journal of the Acoustical Society of America.

[21]  Robert Leech,et al.  Overlapping Networks Engaged during Spoken Language Production and Its Cognitive Control , 2014, The Journal of Neuroscience.

[22]  Robert J. Zatorre,et al.  Neural networks involved in voluntary and involuntary vocal pitch regulation in experienced singers , 2010, Neuropsychologia.

[23]  V. Gracco,et al.  Perceptual recalibration of speech sounds following speech motor learning. , 2009, The Journal of the Acoustical Society of America.

[24]  S. Blakemore,et al.  Action prediction in the cerebellum and in the parietal lobe , 2003, Experimental Brain Research.

[25]  Daniel R. Lametti,et al.  Plasticity in the Human Speech Motor System Drives Changes in Speech Perception , 2014, The Journal of Neuroscience.

[26]  Michael I. Jordan,et al.  Sensorimotor adaptation of speech I: Compensation and adaptation. , 2002, Journal of speech, language, and hearing research : JSLHR.

[27]  D M Wolpert,et al.  Multiple paired forward and inverse models for motor control , 1998, Neural Networks.

[28]  T. Ilić,et al.  Transcranial direct current stimulation , 2008, Clinical Neurophysiology.

[29]  V. Della-Maggiore,et al.  Sensorimotor Adaptation , 2015, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[30]  David J. Ostry,et al.  Auditory plasticity and speech motor learning , 2009, Proceedings of the National Academy of Sciences.

[31]  Roman Rolke,et al.  Transcranial direct current stimulation of the motor cortex induces distinct changes in thermal and mechanical sensory percepts , 2010, Clinical Neurophysiology.

[32]  Jeffery A. Jones,et al.  Remapping Auditory-Motor Representations in Voice Production , 2005, Current Biology.

[33]  Cathy J. Price,et al.  Functional Heterogeneity within the Default Network during Semantic Processing and Speech Production , 2012, Front. Psychology.

[34]  Ethan R. Buch,et al.  Effects of tDCS on motor learning and memory formation: A consensus and critical position paper , 2016, Clinical Neurophysiology.

[35]  Scott T. Grafton,et al.  Forward modeling allows feedback control for fast reaching movements , 2000, Trends in Cognitive Sciences.

[36]  J. Elman.  Effects of frequency-shifted feedback on the pitch of vocal productions. , 1981, The Journal of the Acoustical Society of America.

[37]  N Accornero,et al.  Polarization of the human motor cortex through the scalp , 1998, Neuroreport.

[38]  Richard G. Swensson,et al.  The elusive tradeoff: Speed vs accuracy in visual discrimination tasks , 1972 .

[39]  Jeffery A. Jones,et al.  Perceptual calibration of F0 production: evidence from feedback perturbation. , 2000, The Journal of the Acoustical Society of America.

[40]  P. Matthews,et al.  Semantic Processing in the Left Inferior Prefrontal Cortex: A Combined Functional Magnetic Resonance Imaging and Transcranial Magnetic Stimulation Study , 2003, Journal of Cognitive Neuroscience.

[41]  P. D. Eimas,et al.  Selective adaptation of linguistic feature detectors , 1973 .

[42]  M. Koslowsky,et al.  tDCS polarity effects in motor and cognitive domains: a meta-analytical review , 2011, Experimental Brain Research.

[43]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[44]  Steven Mark Miller,et al.  The use of tDCS and CVS as methods of non-invasive brain stimulation , 2007, Brain Research Reviews.

[45]  Fatemeh Mollaei,et al.  Sensorimotor adaptation of speech in Parkinson's disease , 2013, Movement disorders : official journal of the Movement Disorder Society.

[46]  Leonardo Fogassi,et al.  The inferior parietal lobule: where action becomes perception. , 2006, Novartis Foundation symposium.

[47]  Sang Ho Ahn,et al.  Primary motor cortex activation by transcranial direct current stimulation in the human brain , 2008, Neuroscience Letters.

[48]  Felipe Fregni,et al.  Updates on the use of non-invasive brain stimulation in physical and rehabilitation medicine. , 2009, Journal of rehabilitation medicine.

[49]  Richard S. J. Frackowiak,et al.  Differential activation of right and left posterior sylvian regions by semantic and phonological tasks: a positron-emission tomography study in normal human subjects , 1994, Neuroscience Letters.

[50]  Robert J. Zatorre,et al.  Experience-dependent neural substrates involved in vocal pitch regulation during singing , 2008, NeuroImage.

[51]  Michael I. Jordan,et al.  Sensorimotor adaptation in speech production. , 1998, Science.

[52]  K. Munhall,et al.  Compensation following real-time manipulation of formants in isolated vowels. , 2006, The Journal of the Acoustical Society of America.

[53]  D. Henriques,et al.  Sensory recalibration of hand position following visuomotor adaptation. , 2009, Journal of neurophysiology.

[54]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[55]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[56]  V. Gracco,et al.  Sensorimotor integration for speech motor learning involves the inferior parietal cortex , 2011, The European journal of neuroscience.

[57]  Robert Leech,et al.  The contribution of the inferior parietal cortex to spoken language production , 2012, Brain and Language.