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Experimental Brain Research

, Volume 237, Issue 6, pp 1539–1549 | Cite as

Bihemispheric anodal transcranial direct-current stimulation over temporal cortex enhances auditory selective spatial attention

  • Jörg LewaldEmail author
Research Article
  • 61 Downloads

Abstract

The capacity to selectively focus on a particular speaker of interest in a complex acoustic environment with multiple persons speaking simultaneously—a so-called “cocktail-party” situation—is of decisive importance for human verbal communication. Here, the efficacy of single-dose transcranial direct-current stimulation (tDCS) in improving this ability was tested in young healthy adults (n = 24), using a spatial task that required the localization of a target word in a simulated “cocktail-party” situation. In a sham-controlled crossover design, offline bihemispheric double-monopolar anodal tDCS was applied for 30 min at 1 mA over auditory regions of temporal lobe, and the participant’s performance was assessed prior to tDCS, immediately after tDCS, and 1 h after tDCS. A significant increase in the amount of correct localizations by on average 3.7 percentage points (d = 1.04) was found after active, relative to sham, tDCS, with only insignificant reduction of the effect within 1 h after tDCS offset. Thus, the method of bihemispheric tDCS could be a promising tool for enhancement of human auditory attentional functions that are relevant for spatial orientation and communication in everyday life.

Keywords

Sound localization Cocktail-party effect Selective spatial attention Auditory segregation Bihemispheric transcranial direct-current stimulation 

Notes

Acknowledgements

The author wishes to thank Anna Aust and Emily Eckhardt for data collection, Alina Shamayeva and Michael-Christian Schlüter for help in running the experiments, and Peter Dillmann for preparing the software and parts of the electronic equipment. This work was supported by the German Federal Ministry of Education and Research in the framework of the TRAIN-STIM project (Grant number 01GQ1424E).

Compliance with ethical standards

Conflict of interest

The author declares that he has no conflict of interest.

References

  1. Ahveninen J, Jääskeläinen IP, Raij T, Bonmassar G, Devore S, Hämäläinen M, Levänen S, Lin FH, Sams M, Shinn-Cunningham BG, Witzel T, Belliveau JW (2006) Task-modulated “what” and “where” pathways in human auditory cortex. Proc Natl Acad Sci USA 103:14608–14613CrossRefGoogle Scholar
  2. Alain C, Arnott SR, Hevenor S, Graham S, Grady CL (2001) ‘What’ and ‘where’ in the human auditory system. Proc Natl Acad Sci USA 98:12301–12306CrossRefGoogle Scholar
  3. Antal A, Nitsche MA, Kruse W, Kincses TZ, Hoffmann K-P, Paulus W (2004) Direct current stimulation over V5 enhances visuomotor coordination by improving motion perception in humans. J Cogn Neurosci 16:521–527CrossRefGoogle Scholar
  4. Arnott SR, Binns MA, Grady CL, Alain C (2004) Assessing the auditory dual-pathway model in humans. NeuroImage 22:401–408CrossRefGoogle Scholar
  5. Baudewig J, Nitsche MA, Paulus W, Frahm J (2001) Regional modulation of BOLD MRI responses to human sensorimotor activation by transcranial direct current stimulation. Magn Res Med 45:196–201CrossRefGoogle Scholar
  6. Boggio PS, Nunes A, Rigonatti SP, Nitsche MA, Pascual-Leone A, Fregni F (2007) Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restor Neurol Neurosci 25:123–129Google Scholar
  7. Boggio PS, Rigonatti SP, Ribeiro RB, Myczkowski ML, Nitsche MA, Pascual-Leone A, Fregni F (2008) A randomized, double-blind clinical trial on the efficacy of cortical direct current stimulation for the treatment of major depression. Int J Neuropsychopharmacol 11:249–254CrossRefGoogle Scholar
  8. Brunoni AR, Zanao TA, Ferrucci R, Priori A, Valiengo L, de Oliveira JF, Boggio PS, Lotufo PA, Benseñor IM, Fregni F (2013) Bifrontal tDCS prevents implicit learning acquisition in antidepressant-free patients with major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry 43:146–150CrossRefGoogle Scholar
  9. Cherry E (1953) Some experiments on the recognition of speech with one and with two ears. J Acoust Soc Am 25:975–979CrossRefGoogle Scholar
  10. Derey K, Valente G, de Gelder B, Formisano E (2016) Opponent coding of sound location (azimuth) in planum temporale is robust to sound-level variations. Cereb Cortex 26:450–464CrossRefGoogle Scholar
  11. Faul F, Erdfelder E, Lang AG, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39:175–191CrossRefGoogle Scholar
  12. Fiori V, Nitsche M, Iasevoli L, Cucuzza G, Caltagirone C, Marangolo P (2017) Differential effects of bihemispheric and unihemispheric transcranial direct current stimulation in young and elderly adults in verbal learning. Behav Brain Res 321:170–175CrossRefGoogle Scholar
  13. Fricke K, Seeber AA, Thirugnanasambandam N, Paulus W, Nitsche MA, Rothwell JC (2011) Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. J Neurophysiol 105:1141–1149CrossRefGoogle Scholar
  14. Gazzaley A, Cooney JW, Rissman J, D’Esposito M (2005) Top-down suppression deficit underlies working memory impairment in normal aging. Nat Neurosci 8:1298–1300CrossRefGoogle Scholar
  15. Guski R (1990) Auditory localization: effects of reflecting surfaces. Perception 19:819–830CrossRefGoogle Scholar
  16. Hanenberg C, Getzmann S, Lewald J (2017) Can DC stimulation enhance selective auditory spatial attention in cocktail-party situations? A combined tDCS, ERP and psychophysics study. Neuroforum 23(Suppl):T24-4AGoogle Scholar
  17. van der Heijden K, Rauschecker JP, Formisano E, Valente G, de Gelder B (2018) Active sound localization sharpens spatial tuning in human primary auditory cortex. J Neurosci 38:8574–8587CrossRefGoogle Scholar
  18. Heimrath K, Breitling C, Krauel K, Heinze H-J, Zaehle T (2015) Modulation of pre-attentive spectro-temporal feature processing in the human auditory system by HD-tDCS. Eur J Neurosci 41:1580–1586CrossRefGoogle Scholar
  19. Heimrath K, Kuehne M, Heinze H-J, Zaehle T (2014) Transcranial direct current stimulation (tDCS) traces the predominance of the left auditory cortex for processing of rapidly changing acoustic information. Neuroscience 261:68–73CrossRefGoogle Scholar
  20. Huang YZ, Lu MK, Antal A, Classen J, Nitsche M, Ziemann U, Ridding M, Hamada M, Ugawa Y, Jaberzadeh S, Suppa A, Paulus W, Rothwell J (2017) Plasticity induced by non-invasive transcranial brain stimulation: a position paper. Clin Neurophysiol 128:2318–2329CrossRefGoogle Scholar
  21. Impey D, Knott V (2015) Effect of transcranial direct current stimulation (tDCS) on MMN-indexed auditory discrimination: a pilot study. J Neural Transm 122:1175–1185CrossRefGoogle Scholar
  22. Jacobson L, Koslowsky M, Lavidor M (2012) tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp Brain Res 216:1–10CrossRefGoogle Scholar
  23. Kessler SK, Turkeltaub PE, Benson JG, Hamilton RH (2012) Differences in the experience of active and sham transcranial direct current stimulation. Brain Stimul 5:155–162CrossRefGoogle Scholar
  24. Klein E, Mann A, Huber S, Bloechle J, Willmes K, Karim AA, Nuerk H-C, Moeller K (2013) Bilateral bi-cephalic tDCS with two active electrodes of the same polarity modulates bilateral cognitive processes differentially. PLoS One 8:e71607CrossRefGoogle Scholar
  25. von Kriegstein K, Griffiths TD, Thompson SK, McAlpine D (2008) Responses to interaural time delay in human cortex. J Neurophysiol 100:2712–2718CrossRefGoogle Scholar
  26. Kuo M-F, Polanía R, Nitsche M (2016) Physiology of transcranial direct and alternating current stimulation. In: Brunoni A, Nitsche M, Loo C (eds) Transcranial direct current stimulation in neuropsychiatric disorders: clinical principles and management. Springer, BaselGoogle Scholar
  27. Ladeira A, Fregni F, Campanhã C, Valasek CA, De Ridder D, Brunoni AR, Boggio PS (2011) Polarity-dependent transcranial direct current stimulation effects on central auditory processing. PLoS One 6:e25399CrossRefGoogle Scholar
  28. Lang N, Siebner HR, Ward NS, Lee L, Nitsche MA, Paulus W, Rothwell JC, Lemon RN, Frackowiak RS (2005) How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci 22:495–504CrossRefGoogle Scholar
  29. Lee CC, Middlebrooks JC (2011) Auditory cortex spatial sensitivity sharpens during task performance. Nat Neurosci 14:108–114CrossRefGoogle Scholar
  30. Lewald J (2016) Modulation of human auditory spatial scene analysis by transcranial direct current stimulation. Neuropsychologia 84:282–293CrossRefGoogle Scholar
  31. Lewald J, Getzmann S (2015) Electrophysiological correlates of cocktail-party listening. Behav Brain Res 292:157–166CrossRefGoogle Scholar
  32. Lewald J, Hanenberg C, Getzmann S (2016) Brain correlates of the orientation of auditory spatial attention onto speaker location in a “cocktail-party” situation. Psychophysiology 53:1484–1495CrossRefGoogle Scholar
  33. Lewald J, Hausmann M (2013) Effects of sex and age on auditory spatial scene analysis. Hear Res 299:46–52CrossRefGoogle Scholar
  34. Lewald J, Meister IG, Weidemann J, Töpper R (2004a) Involvement of the superior temporal cortex and the occipital cortex in spatial hearing: evidence from repetitive transcranial magnetic stimulation. J Cogn Neurosci 16:828–838CrossRefGoogle Scholar
  35. Lewald J, Wienemann M, Boroojerdi B (2004b) Shift in sound localization induced by rTMS of the posterior parietal lobe. Neuropsychologia 42:1598–1607CrossRefGoogle Scholar
  36. Liebetanz D, Nitsche MA, Tergau F, Paulus W (2002) Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain 125:2238–2247CrossRefGoogle Scholar
  37. Lindenberg R, Nachtigall L, Meinzer M, Sieg MM, Flöel A (2013) Differential effects of dual and unihemispheric motor cortex stimulation in older adults. J Neurosci 33:9176–9183CrossRefGoogle Scholar
  38. Loui P, Hohmann A, Schlaug G (2010) Inducing disorders in pitch perception and production: a reverse-engineering approach. Proc Meet Acoust 9:50002CrossRefGoogle Scholar
  39. Magezi DA, Krumbholz K (2010) Evidence for opponent-channel coding of interaural time differences in human auditory cortex. J Neurophysiol 104:1997–2007CrossRefGoogle Scholar
  40. Martin DM, Liu R, Alonzo A, Green M, Player MJ, Sachdev P, Loo CK (2013) Can transcranial direct current stimulation enhance outcomes from cognitive training? A randomized controlled trial in healthy participants. Int J Neuropsychopharmacol 16:1927–1936CrossRefGoogle Scholar
  41. Mathys C, Loui P, Zheng X, Schlaug G (2010) Non-invasive brain stimulation applied to Heschl’s gyrus modulates pitch discrimination. Front Psychol 1:193CrossRefGoogle Scholar
  42. McFadden JL, Borckardt JJ, George MS, Beam W (2011) Reducing procedural pain and discomfort associated with transcranial direct current stimulation. Brain Stimul 4:38–42CrossRefGoogle Scholar
  43. Meinzer M, Jähnigen S, Copland DA, Darkow R, Grittner U, Avirame K, Rodriguez AD, Lindenberg R, Flöel A (2014) Transcranial direct current stimulation over multiple days improves learning and maintenance of a novel vocabulary. Cortex 50:137–147CrossRefGoogle Scholar
  44. Meinzer M, Lindenberg R, Antonenko D, Flaisch T, Flöel A (2013) Anodal transcranial direct current stimulation temporarily reverses age-associated cognitive decline and functional brain activity changes. J Neurosci 33:12470–12478CrossRefGoogle Scholar
  45. Miller LM, Recanzone GH (2009) Populations of auditory cortical neurons can accurately encode acoustic space across stimulus intensity. Proc Natl Acad Sci USA 106:5931–5935CrossRefGoogle Scholar
  46. Miniussi C, Harris JA, Ruzzoli M (2013) Modelling non-invasive brain stimulation in cognitive neuroscience. Neurosci Biobehav Rev 37:1702–1712CrossRefGoogle Scholar
  47. Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, Nitsche MA (2013) Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul 6:424–432CrossRefGoogle Scholar
  48. Monte-Silva K, Kuo M-F, Liebetanz D, Paulus W, Nitsche MA (2010) Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). J Neurophysiol 103:1735–1740CrossRefGoogle Scholar
  49. Naros G, Geyer M, Koch S, Mayr L, Ellinger T, Grimm F, Gharabaghi A (2016) Enhanced motor learning with bilateral transcranial direct current stimulation: impact of polarity or current flow direction? Clin Neurophysiol 127:2119–2126CrossRefGoogle Scholar
  50. Nasseri P, Nitsche MA, Ekhtiari H (2015) A framework for categorizing electrode montages in transcranial direct current stimulation. Front Hum Neurosci 9:54CrossRefGoogle Scholar
  51. Nelson JT, McKinley R, Golob EJ, Warm JS, Parasuraman R (2014) Enhancing vigilance in operators with pre frontal cortex transcranial direct current stimulation (tDCS). NeuroImage 85:909–917CrossRefGoogle Scholar
  52. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art. Brain Stimul 1:206–223CrossRefGoogle Scholar
  53. Nitsche MA, Doemkes S, Karaköse T, Antal A, Liebetanz D, Lang N, Tergau F, Paulus W (2007) Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 97:3109–3117CrossRefGoogle Scholar
  54. Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633–639CrossRefGoogle Scholar
  55. Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899–1901CrossRefGoogle Scholar
  56. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefGoogle Scholar
  57. Palm U, Reisinger E, Keeser D, Kuo MF, Pogarell O, Leicht G, Mulert C, Nitsche MA, Padberg F (2013) Evaluation of sham transcranial direct current stimulation for randomized, placebo-controlled clinical trials. Brain Stimul 6:690–695CrossRefGoogle Scholar
  58. Perceval G, Flöel A, Meinzer M (2016) Can transcranial direct current stimulation counteract age-associated functional impairment? Neurosci Biobehav Rev 65:157–172CrossRefGoogle Scholar
  59. Priori A, Berardelli A, Rona S, Accornero N, Manfredi M (1998) Polarization of the human motor cortex through the scalp. NeuroReport 9:2257–2260CrossRefGoogle Scholar
  60. Rauschecker JP (2018) Where, when, and how: are they all sensorimotor? Towards a unified view of the dorsal pathway in vision and audition. Cortex 98:262–268CrossRefGoogle Scholar
  61. Russo R, Wallace D, Fitzgerald PB, Cooper NR (2013) Perception of comfort during active and sham transcranial direct current stimulation: a double blind study. Brain Stimul 6:946–951CrossRefGoogle Scholar
  62. Salminen NH, Tiitinen H, May PJC (2012) Auditory spatial processing in the human cortex. Neuroscientist 18:602–612CrossRefGoogle Scholar
  63. Salminen NH, Tiitinen H, Miettinen I, Alku P, May PJ (2010) Asymmetrical representation of auditory space in human cortex. Brain Res 1306:93–99CrossRefGoogle Scholar
  64. Sherbecoe RL, Studebaker GA (2004) Supplementary formulas and tables for calculating and interconverting speech recognition scores in transformed arcsine units. Int J Audiol 43:442–448CrossRefGoogle Scholar
  65. Stagg CJ, Lin RL, Mezue M, Segerdahl A, Kong Y, Xie J, Tracey I (2013) Widespread modulation of cerebral perfusion induced during and after transcranial direct current stimulation applied to the left dorsolateral prefrontal cortex. J Neurosci 33:11425–11431CrossRefGoogle Scholar
  66. Stagg CJ, Nitsche MA (2011) Physiological basis of transcranial direct current stimulation. Neuroscientist 17:37–53CrossRefGoogle Scholar
  67. Stagg CJ, O’Shea J, Kincses ZT, Woolrich M, Matthews PM, Johansen-Berg H (2009) Modulation of movement-associated cortical activation by transcranial direct current stimulation. Eur J Neurosci 30:1412–1423CrossRefGoogle Scholar
  68. Studebaker GA (1985) A “rationalized” arcsine transform. J Speech Hear Res 28:455–462CrossRefGoogle Scholar
  69. Tang MF, Hammond GR (2013) Anodal transcranial direct current stimulation over auditory cortex degrades frequency discrimination by affecting temporal, but not place, coding. Eur J Neurosci 38:2802–2811CrossRefGoogle Scholar
  70. Tang MF, Hammond GR, Badcock DR (2016) Are participants aware of the type and intensity of transcranial direct current stimulation? PLoS One 11:e0148825CrossRefGoogle Scholar
  71. Tatti E, Rossi S, Innocenti I, Rossi A, Santarnecchi E (2016) Non-invasive brain stimulation of the aging brain: state of the art and future perspectives. Ageing Res Rev 29:66–89CrossRefGoogle Scholar
  72. Vines BW, Cerruti C, Schlaug G (2008) Dual-hemisphere tDCS facilitates greater improvements for healthy subjects’ non-dominant hand compared to uni-hemisphere stimulation. BMC Neurosci 9:103CrossRefGoogle Scholar
  73. Wagner S, Rampersad SM, Aydin Ü, Vorwerk J, Oostendorp TF, Neuling T, Herrmann CS, Stegeman DF, Wolters CH (2014) Investigation of tDCS volume conduction effects in a highly realistic head model. J Neural Eng 11:016002CrossRefGoogle Scholar
  74. Werner-Reiss U, Groh JM (2008) A rate code for sound azimuth in monkey auditory cortex: implications for human neuroimaging studies. J Neurosci 28:3747–3758CrossRefGoogle Scholar
  75. 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 127:1031–1048CrossRefGoogle Scholar
  76. Woods TM, Lopez SE, Long JH, Rahman JE, Recanzone GH (2006) Effects of stimulus azimuth and intensity on the single-neuron activity in the auditory cortex of the alert macaque monkey. J Neurophysiol 96:3323–3337CrossRefGoogle Scholar
  77. Wöstmann M, Vosskuhl J, Obleser J, Herrmann CS (2018) Opposite effects of lateralised transcranial alpha versus gamma stimulation on auditory spatial attention. Brain Stimul 11:752–758CrossRefGoogle Scholar
  78. Zaehle T, Beretta M, Jäncke L, Herrmann CS, Sandmann P (2011) Excitability changes induced in the human auditory cortex by transcranial direct current stimulation: direct electrophysiological evidence. Exp Brain Res 215:135–140CrossRefGoogle Scholar
  79. Zhang X, Zhang Q, Hu X, Zhang B (2015) Neural representation of three-dimensional acoustic space in the human temporal lobe. Front Hum Neurosci 9:203Google Scholar
  80. Zheng X, Alsop DC, Schlaug G (2011) Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. Neuroimage 58:26–33CrossRefGoogle Scholar
  81. Zündorf IC, Karnath H-O, Lewald J (2011) Male advantage in sound localization at cocktail parties. Cortex 47:741–749CrossRefGoogle Scholar
  82. Zündorf IC, Karnath H-O, Lewald J (2014) The effect of brain lesions on sound localization in complex acoustic environments. Brain 137:1410–1418CrossRefGoogle Scholar
  83. Zündorf IC, Lewald J, Karnath H-O (2013) Neural correlates of sound localization in complex acoustic environments. PLoS One 8:e64259CrossRefGoogle Scholar
  84. Zündorf IC, Lewald J, Karnath H-O (2016) Testing the dual-pathway model for auditory processing in human cortex. Neuroimage 124:672–681CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Auditory Cognitive Neuroscience Laboratory, Department of Cognitive Psychology, Faculty of PsychologyRuhr University BochumBochumGermany
  2. 2.Leibniz Research Centre for Working Environment and Human FactorsDortmundGermany

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