Abstract
Neural interactions between sensorimotor integration mechanisms play critical roles in voice motor control. We investigated how high-definition transcranial direct current stimulation (HD-tDCS) of the left ventral motor cortex modulates neural mechanisms of sensorimotor integration during voice motor control. HD-tDCS was performed during speech vowel production in an altered auditory feedback (AAF) paradigm in response to upward and downward pitch-shift stimuli. In one experiment, two groups received either anodal or cathodal 2 milliamp (mA) HD-tDCS to the left ventral motor cortex while a third group received sham (placebo) stimulation. In a second experiment, two groups received either 1 mA or 2 mA cathodal HD-tDCS to the left ventral motor cortex. Results of the first experiment indicated that the magnitude of vocal compensation was significantly reduced following anodal and cathodal HD-tDCS only in responses to downward pitch-shift AAF stimuli, with stronger effects associated with cathodal HD-tDCS. However, no such effect was observed following sham stimulation. Results of the second experiment indicate that there is not a differential effect of modulation from 1 mA versus 2 mA. Further, these results replicate the directional finding of the first experiment for vocal compensation in response to downward pitch-shift only. These findings suggest that neurostimulation of the left ventral motor cortex modulates sensorimotor mechanisms underlying voice motor control. We speculate that this effect is associated with the increased contribution of feedforward motor mechanisms, leading to reduced compensatory speech responses to AAF.
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References
Behroozmand R, Korzyukov O, Sattler L, Larson CR (2012) Opposing and following vocal responses to pitch-shifted auditory feedback: Evidence for different mechanisms of voice pitch control. J Acoust Soc Am 132:2468–2477. https://doi.org/10.1121/1.4746984
Behroozmand R, Ibrahim N, Korzyukov O, Robin DA, Larson CR (2014) Left-hemisphere activation is associated with enhanced vocal pitch error detection in musicians with absolute pitch. Brain Cogn 84:97–108. https://doi.org/10.1016/j.bandc.2013.11.007
Behroozmand R, Ibrahim N, Korzyukov O, Robin DA, Larson CR (2015a) Functional role of delta and theta band oscillations for auditory feedback processing during vocal pitch motor control. Front Neurosci. https://doi.org/10.3389/Fnins.2015.00109
Behroozmand R, Shebek R, Hansen DR, Oya H, Robin DA, Howard Iii MA, Greenlee JDW (2015b) Sensory–motor networks involved in speech production and motor control: an fMRI study. Neuroimage. https://doi.org/10.1016/j.neuroimage.2015.01.040
Bikson M, Grossman P, Thomas C, Zannou AL, Jiang J, Adnan T, Mourdoukoutas AP, Kronberg G, Truong D, Boggio P, Brunoni AR, Charvet L, Fregni F, Fritsch B, Gillick B, Hamilton RH, Hampstead BM, Jankord R, Kirton A, Knotkova H, Liebetanz D, Liu A, Loo C, Nitsche MA, Reis J, Richardson JD, Rotenberg A, Turkeltaub PE, Woods AJ (2016) Safety of Transcranial direct current stimulation: evidence based update 2016. Brain Stimul. https://doi.org/10.1016/j.brs.2016.06.004
Boersma P, Weenink D (2015) Praat: doing phonetics by computer [Computer program]. Version 5.4.09, retrieved 1 June 2015 from https://www.praat.org/
Caparelli-Daquer EM, Zimmermann TJ, Mooshagian E, Parra LC, Rice JK, Datta A, Bikson M, Wassermann EMI (2012) A pilot study on effects of 4x1 high-definition tDCS on Motor Cortex excitability, 2012 annual international conference of the ieee engineering in medicine and biology society, pp 735–738
Chen SH, Liu HJ, Xu Y, Larson CR (2007) Voice F(0) responses to pitch-shifted voice feedback during English speech. J Acoust Soc Am 121:1157–1163. https://doi.org/10.1121/1.2404624
Chhetri DK, Neubauer J, Sofer E, Berry DA (2014) Influence and interactions of laryngeal adductors and cricothyroid muscles on fundamental frequency and glottal posture control. J Acoust Soc Am 135:2052–2064. https://doi.org/10.1121/1.4865918
Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M (2009) Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimul Basic Transl Clin Res Neuromodul 2:201–207.e1. https://doi.org/10.1016/j.brs.2009.03.005
Dockery CA, Hueckel-Weng R, Birbaumer N, Plewnia C (2009) Enhancement of planning ability by transcranial direct current stimulation. J Neurosci 29:7271–7277. https://doi.org/10.1523/jneurosci.0065-09.2009
Flagmeier SG, Ray KL, Parkinson AL, Li K, Vargas R, Price LR, Laird AR, Larson CR, Robin DA (2014) The neural changes in connectivity of the voice network during voice pitch perturbation. Brain Lang 132:7–13. https://doi.org/10.1016/j.bandl.2014.02.001
Franklin DW, Wolpert DM (2011) Computational mechanisms of sensorimotor control. Neuron 72:425–442. https://doi.org/10.1016/j.neuron.2011.10.006
Garnett EO, Den Ouden D-B (2015) Validating a sham condition for use in high definition transcranial direct current stimulation. Brain Stimul 8:551–554. https://doi.org/10.1016/j.brs.2015.01.399
Garnett EO, Malyutina S, Datta A, Den Ouden DB (2015) On the use of the terms anodal and cathodal in high-definition transcranial direct current stimulation: a technical note. Neuromodulation. https://doi.org/10.1111/ner.12320
Gentil M, Chauvin P, Pinto S, Pollak P, Benabid AL (2001) Effect of bilateral stimulation of the subthalamic nucleus on parkinsonian voice. Brain Lang 78:233–240. https://doi.org/10.1006/brln.2001.2466
Guenther FH (2006) Cortical interactions underlying the production of speech sounds. J Commun Disord 39:350–365. https://doi.org/10.1016/j.jcomdis.2006.06.013
Guenther FH, Ghosh SS, Tourville JA (2006) Neural modeling and imaging of the cortical interactions underlying syllable production. Brain Lang 96:280–301. https://doi.org/10.1016/j.bandl.2005.06.001
Hickok G, Poeppel D (2007) Opinion-the cortical organization of speech processing. Nat Rev Neurosci 8:393–402. https://doi.org/10.1038/Nrn2113
Holland R, Crinion J (2012) Can tDCS enhance treatment of aphasia after stroke? Aphasiology 26:1169–1191. https://doi.org/10.1080/02687038.2011.616925
Holland R, Leff AP, Penny WD, Rothwell JC, Crinion J (2016) Modulation of frontal effective connectivity during speech. Neuroimage 140:126–133. https://doi.org/10.1016/j.neuroimage.2016.01.037
Houde JF, Chang EF (2015) The cortical computations underlying feedback control in vocal production. Curr Opin Neurobiol 33:174–181. https://doi.org/10.1016/j.conb.2015.04.006
Houde JF, Nagarajan SS (2011) Speech production as state feedback control. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2011.00082
Huang XY, Chen X, Yan N, Jones JA, Wang EQ, Chen L, Guo ZQ, Li WF, Liu P, Liu HJ (2016) The impact of parkinson's disease on the cortical mechanisms that support auditory-motor integration for voice control. Hum Brain Map 37:4248–4261. https://doi.org/10.1002/hbm.23306
Hummel F, Celnik P, Giraux P, Floel A, Wu WH, Gerloff C, Cohen LG (2005) Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128:490–499. https://doi.org/10.1093/brain/awh369
Iyer MB, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann EM (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64:872–875
Jacobson L, Koslowsky M, Lavidor M (2012) tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp Brain Res 216:1–10. https://doi.org/10.1007/s00221-011-2891-9
Jones JA, Keough D (2008) Auditory-motor mapping for pitch control in singers and nonsingers. Exp Brain Res 190:279–287. https://doi.org/10.1007/s00221-008-1473-y
Kumar V, Croxson PL, Simonyan K (2016) Structural organization of the laryngeal motor cortical network and its implication for evolution of speech production. J Neurosci 36:4170–4181. https://doi.org/10.1523/jneurosci.3914-15.2016
Kuo HI, Bikson M, Datta A, Minhas P, Paulus W, Kuo MF, Nitsche MA (2013) Comparing cortical plasticity induced by conventional and high-definition 4 x 1 ring tDCS: a neurophysiological study. Brain Stimul 6:644–648. https://doi.org/10.1016/j.brs.2012.09.010
Larson CR (1998) Cross-modality influences in speech motor control: The use of pitch shifting for the study of F0 control. J Commun Disord 31:489–503. https://doi.org/10.1016/S0021-9924(98)00021-5
Liu HJ, Behroozmand R, Bove M, Larson CR (2011) Laryngeal electromyographic responses to perturbations in voice pitch auditory feedback. J Acoust Soc Am 129:3946–3954. https://doi.org/10.1121/1.3575593
Marshall L, Molle M, Siebner HR, Born J (2005) Bifrontal transcranial direct current stimulation slows reaction time in a working memory task. BMC Neurosci. https://doi.org/10.1186/1471-2202-6-23
Monti A, Cogiamanian F, Marceglia S, Ferrucci R, Mameli F, Mrakic-Sposta S, Vergari M, Zago S, Priori A (2008) Improved naming after transcranial direct current stimulation in aphasia. J Neurol Neurosurg Psychiatry 79:451–453. https://doi.org/10.1136/jnnp.2007.135277
Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol Lond 527:633–639. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00633.x
Parkinson AL, Behroozmand R, Ibrahim N, Korzyukov O, Larson CR, Robin DA (2014) Effective connectivity associated with auditory error detection in musicians with absolute pitch. Front Neurosci. https://doi.org/10.3389/Fnins.2014.00046
Rahman A, Reato D, Arlotti M, Gasca F, Datta A, Parra LC, Bikson M (2013) Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. J Physiol Lond 591:2563–2578. https://doi.org/10.1113/jphysiol.2012.247171
Ransmayr G (2011) Physical, occupational, speech and swallowing therapies and physical exercise in Parkinson's disease. J Neural Transmission 118:773–781. https://doi.org/10.1007/s00702-011-0622-9
Rauschecker JP (2011) An expanded role for the dorsal auditory pathway in sensorimotor control and integration. Hear Res 271:16–25. https://doi.org/10.1016/j.heares.2010.09.001
Rauschecker JP, Scott SK (2009) Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12:718–724. https://doi.org/10.1038/nn.2331
Simonyan K, Horwitz B (2011) Laryngeal motor cortex and control of speech in humans. Neuroscientist 17:197–208. https://doi.org/10.1177/1073858410386727
Skodda S, Gronheit W, Schlegel U (2012a) Impairment of vowel articulation as a possible marker of disease progression in parkinson's disease. PLoS ONE. https://doi.org/10.1371/journal.pone.0032132
Skodda S, Schlegel U, Südmeyer M, Schnitzler A, Wojtecki L (2012b) Effects of levodopa and deep brain stimulation on motor speech performance in Parkinson’s disease. Basal Ganglia 2:49–54. https://doi.org/10.1016/j.baga.2012.01.001
Skodda S, Groenheit W, Mancinelli N, Schlegel U (2013) Progression of voice and speech impairment in the course of parkinson's disease: a longitudinal study. Parkinsons Dis. https://doi.org/10.1155/2013/389195
Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11:R729–R732. https://doi.org/10.1016/s0960-9822(01)00432-8
Wolpert DM, Diedrichsen J, Flanagan JR (2011) Principles of sensorimotor learning. Nat Rev Neurosci 12:739–751. https://doi.org/10.1038/nrn3112
Woods AJ, Antal A, Bikson M, Boggio PS, Brunoni AR, Celnik P, Cohen LG, Fregni F, Herrmann CS, Kappenman ES, Knotkova H, Liebetanz D, Miniussi C, Miranda PC, Paulus W, Priori A, Reato D, Stagg C, Wenderoth N, Nitsche MA (2016) A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol 127:1031–1048. https://doi.org/10.1016/j.clinph.2015.11.012
Zarate JM (2013) The neural control of singing. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2013.00237
Acknowledgements
The authors would like to thank Dr. Julius Fridriksson for access to the MxN HD-tDCS stimulation device, and Janelle Rocktashel for assistance with experiment 2.
Funding
This research was supported by a Magellan scholarship award to K.B. and C.H., from the office of the Vice President for Research at the University of South Carolina (Grant number: 11560–15-38104).
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RB and DDO designed the research, and KB, CH, and DF collected data for the experiments. RB, DdO, KJ, and DF analyzed the collected data. RB and DDO wrote the paper and all authors reviewed and approved the final draft.
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The study was approved by the institutional Review Board of the University of South Carolina (Experiment 1: Pro00040909; Experiment 2: Pro00059310) and performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments.
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All subjects gave written consent to participate and were either monetarily compensated (Experiment 1) or received course credit (Experiments 1 and 2) for their participation.
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The data that support the findings of this study are available from the corresponding author, DdO, upon reasonable request.
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Communicated by Winston D. Byblow.
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Behroozmand, R., Johari, K., Bridwell, K. et al. Modulation of vocal pitch control through high-definition transcranial direct current stimulation of the left ventral motor cortex. Exp Brain Res 238, 1525–1535 (2020). https://doi.org/10.1007/s00221-020-05832-9
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DOI: https://doi.org/10.1007/s00221-020-05832-9