Hostname: page-component-7dd5485656-c8zdz Total loading time: 0 Render date: 2025-10-28T17:26:48.126Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurostimulation and Pupillometry: New Directions for Learning and Research in Applied Linguistics

Published online by Cambridge University Press:  30 June 2020

Nick B. Pandža ,
Ian Phillips ,
Valerie P. Karuzis ,
Polly O'Rourke  and
Stefanie E. Kuchinsky
Nick B. Pandža*
Affiliation:
University of Maryland Applied Research Lab for Intelligence & Security University of Maryland Program in Second Language Acquisition
Ian Phillips
Affiliation:
University of Maryland Applied Research Lab for Intelligence & Security
Valerie P. Karuzis
Affiliation:
University of Maryland Applied Research Lab for Intelligence & Security University of Maryland Program in Measurement, Statistics & Evaluation
Polly O'Rourke
Affiliation:
University of Maryland Applied Research Lab for Intelligence & Security
Stefanie E. Kuchinsky
Affiliation:
University of Maryland Applied Research Lab for Intelligence & Security Walter Reed National Military Medical Center, Audiology and Speech Pathology Center
*
*Corresponding author; E-mail: npandza@umd.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper begins by discussing new trends in the use of neurostimulation techniques in cognitive science and learning research, as well as the nascent research on their application in second language learning. To illustrate this, an experiment designed to investigate the impact of transcutaneous vagus nerve stimulation (tVNS), which is delivered via earbuds, on how learners process and learn Mandarin tones is reported. Pupillometry, which is an index of cognitive effort, is explained and illustrated as one way to assess the impact of tVNS. Participants in the study were native English speakers, naïve to tone languages, pseudorandomly assigned to active or control conditions, while balancing for nonlinguistic pitch ability and musical experience. Their performance after tVNS was assessed using a range of more traditional language outcome measures, including accuracy and reaction times from lexical recognition and recall tasks and was triangulated with pupillometry during word-learning to help understand the mechanism through which tVNS operates. Findings are discussed in light of the literatures on lexical tone learning, cognitive effort, and neurostimulation, including specific benefits for learners of tone languages. Recommendations are made for future work on the increasingly popular area of neurostimulation for the field of applied linguistics in the 40th anniversary issue of ARAL.

Information

Type
Research Article
Information
Annual Review of Applied Linguistics , Volume 40 , March 2020 , pp. 56 - 77
Check for updates
Open Practices
Open materials
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

The experiment in this article earned an Open Materials badge for transparent practices. The data and materials are available at https://www.iris-database.org/iris/app/home/detail?id=york%3a938003&ref=search (Lexical Recall Task & Materials); https://www.iris-database.org/iris/app/home/detail?id=york%3a938002&ref=search (Lexical Recognition Matching & Materials); and https://www.iris-database.org/iris/app/home/detail?id=york%3a938001&ref=search (Passive Word Learning & Materials).

References

Antoniou, M., & Wong, P. C. (2016). Varying irrelevant phonetic features hinders learning of the feature being trained. The Journal of the Acoustical Society of America, 139(1), 271–278.10.1121/1.4939736CrossRefGoogle ScholarPubMed
Aston-Jones, G., & Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28, 403–450.10.1146/annurev.neuro.28.061604.135709CrossRefGoogle ScholarPubMed
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1–48.10.18637/jss.v067.i01CrossRefGoogle Scholar
Bent, T., Bradlow, A. R., & Wright, B. A. (2006). The influence of linguistic experience on the cognitive processing of pitch in speech and nonspeech sounds. Journal of Experimental Psychology: Human Perception and Performance, 32, 97–103.Google ScholarPubMed
Borland, M. S., Engineer, C. T., Vrana, W. A., Moreno, N. A., Engineer, N. D., Vanneste, S., Sharma, P., Pantalia, M. C., Lane, M. C., Rennaker, R. L., & Kilgard, M. P. (2018). The interval between VNS-tone pairings determines the extent of cortical map plasticity. Neuroscience, 369, 76–86.10.1016/j.neuroscience.2017.11.004CrossRefGoogle ScholarPubMed
Borland, M. S., Vrana, W. A., Moreno, N. A., Fogarty, E. A., Buell, E. P., Sharma, P., & Kilgard, M. P. (2016). Cortical map plasticity as a function of vagus nerve stimulation intensity. Brain Stimulation, 9(1), 117–123.10.1016/j.brs.2015.08.018CrossRefGoogle ScholarPubMed
Bowles, A. R., Chang, C. B., & Karuzis, V. P. (2016). Pitch ability as an aptitude for tone learning. Language Learning, 66(4), 774–808.10.1111/lang.12159CrossRefGoogle Scholar
Brysbaert, M., & New, B. (2009). Moving beyond Kučera and Francis: A critical evaluation of current word frequency norms and the introduction of a new and improved word frequency measure for American English. Behavior Research Methods, 41(4), 977–990.10.3758/BRM.41.4.977CrossRefGoogle ScholarPubMed
Brysbaert, M., Warriner, A. B., & Kuperman, V. (2014). Concreteness ratings for 40 thousand generally known English word lemmas. Behavior Research Methods, 46(3), 904–911.10.3758/s13428-013-0403-5CrossRefGoogle ScholarPubMed
Buell, E. P., Loerwald, K. W., Engineer, C. T., Borland, M. S., Buell, J. M., Kelly, C. A., Khan, I. I., Hays, S. A., & Kilgard, M. P. (2018). Cortical map plasticity as a function of vagus nerve stimulation rate. Brain Stimulation, 11(6), 1218–1224.CrossRefGoogle ScholarPubMed
Chandrasekaran, B., Sampath, P. D., & Wong, P. C. M. (2010). Individual variability in cue-weighting and lexical tone learning. Journal of the Acoustical Society of America, 128(1), 456–465.10.1121/1.3445785CrossRefGoogle ScholarPubMed
Colflesh, G., Karuzis, V., & O'Rourke, P. (2016). Effects of working memory training on L2 proficiency and working memory capacity. Proceedings of the Annual Meeting of the Cognitive Science Society, 289–294.Google Scholar
DaSilva, A. F., Truong, D. Q., DosSantos, M. F., Toback, R. L., Datta, A., & Bikson, M. (2015). State-of-art neuroanatomical target analysis of high-definition and conventional tDCS montages used for migraine and pain control. Frontiers in Neuroanatomy, 9, 1–89.CrossRefGoogle ScholarPubMed
Dittinger, E., Barbaroux, M., D'Imperio, M., Jäncke, L., Elmer, S., & Besson, M. (2016). Professional music training and novel word learning: from faster semantic encoding to longer-lasting word representations. Journal of Cognitive Neuroscience, 28(10), 1584–1602.CrossRefGoogle ScholarPubMed
Doughty, C. J., & Long, M. H. (2003). Optimal psycholinguistic environments for distance foreign language learning. Language Learning & Technology, 7(3), 50–80.Google Scholar
Eckstein, M. K., Guerra-Carrillo, B., Singley, A. T. M., & Bunge, S. A. (2017). Beyond eye gaze: What else can eyetracking reveal about cognition and cognitive development? Developmental Cognitive Neuroscience, 25, 69–91.CrossRefGoogle ScholarPubMed
Engineer, N. D., Riley, J. R., Seale, J. D., Vrana, W. A., Shetake, J. A., Sudanagunta, S. P., Borland, M. S., & Kilgard, M. P. (2011). Reversing pathological neural activity using targeted plasticity. Nature, 470(7332), 1–15.10.1038/nature09656CrossRefGoogle ScholarPubMed
Finocchiaro, C., Maimone, M., Brighina, F., Piccoli, T., Giglia, G., & Fierro, B. (2006). A case study of primary progressive aphasia: improvement on verbs after rTMS treatment. Neurocase, 12(6), 317–321.CrossRefGoogle ScholarPubMed
Follesa, P., Biggio, F., Gorini, G., Caria, S., Talani, G., Dazzi, L., Puligheddu, M., Marrosu, F., & Biggio, G. (2007). Vagus nerve stimulation increases norepinephrine concentration and the gene expression of BDNF and bFGF in the rat brain. Brain Research, 1179, 28–34.CrossRefGoogle ScholarPubMed
Frangos, E., Ellrich, J., & Komisaruk, B. R. (2015). Non-invasive access to the vagus nerve central projections via electrical stimulation of the external ear: fMRI evidence in humans. Brain Stimulation, 8(3), 624–636.10.1016/j.brs.2014.11.018CrossRefGoogle ScholarPubMed
George, M. S., & Aston-Jones, G. (2010). Noninvasive techniques for probing neurocircuitry and treating illness: vagus nerve stimulation (VNS), transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). Neuropsychopharmacology, 35(1), 301.CrossRefGoogle Scholar
Gilzenrat, M. S., Nieuwenhuis, S., Jepma, M., & Cohen, J. D. (2010). Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function. Cognitive, Affective, & Behavioral Neuroscience, 10(2), 252–269.Google Scholar
Groves, D. A., Bowman, E. M., & Brown, V. J. (2005). Recordings from the rat locus coeruleus during acute vagal nerve stimulation in the anaesthetised rat. Neuroscience Letters, 379(3), 174–179.CrossRefGoogle ScholarPubMed
Ingvalson, E. M., Ettlinger, M., & Wong, P. C. (2014). Bilingual speech perception and learning: A review of recent trends. International Journal of Bilingualism, 18(1), 35–47.CrossRefGoogle Scholar
Jacobs, H. I., Riphagen, J. M., Razat, C. M., Wiese, S., & Sack, A. T. (2015). Transcutaneous vagus nerve stimulation boosts associative memory in older individuals. Neurobiology of Aging, 36(5), 1860–1867.CrossRefGoogle ScholarPubMed
Kilgard, M. P. (2012). Harnessing plasticity to understand learning and treat disease. Trends in Neurosciences, 35(12), 715–722.CrossRefGoogle ScholarPubMed
Klooster, D. C., de Louw, A. J., Aldenkamp, A. P., Besseling, R. M. H., Mestrom, R. M. C., Carrette, S., Zinger, S., Bergmans, J. W. M., Mess, W. H., Vonck, K., Carrette, E., Breuer, L. E. M., Bernas, A., Tijhuis, A. G., & Boon, P. (2016). Technical aspects of neurostimulation: Focus on equipment, electric field modeling, and stimulation protocols. Neuroscience & Biobehavioral Reviews, 65, 113–141.CrossRefGoogle ScholarPubMed
Kuchinsky, S. E., Ahlstrom, J. B., Vaden, K. I. Jr., Cute, S. L., Humes, L. E., Dubno, J. R., & Eckert, M. A. (2013). Pupil size varies with word listening and response selection difficulty in older adults with hearing loss. Psychophysiology, 50(1), 23–34.CrossRefGoogle Scholar
Kuchinsky, S. E. & Vaden, K. I. Jr. (in press). Aging, hearing loss, and effort: Imaging studies of the aging brain. In Helfer, K. S., Bartlett, E. L., Popper, A. N., & Fay, R. R. (Eds.), The Aging Auditory System. Springer.Google Scholar
Kuipers, J. R., & Thierry, G. (2011). N400 amplitude reduction correlates with an increase in pupil size. Frontiers in Human Neuroscience, 5, 61.CrossRefGoogle ScholarPubMed
Li, M., & DeKeyser, R. (2017). Perception practice, production practice, and musical ability in L2 Mandarin tone-word learning. Studies in Second Language Acquisition, 39(4), 593–620.CrossRefGoogle Scholar
Loewenfeld, I. E. (1999). Otto Lowenstein: Neurologic and ophthalmologic testing methods during his lifetime. Documenta Ophthalmologica, 98(1), 3–20.CrossRefGoogle ScholarPubMed
Manta, S., Dong, J., Debonnel, G., & Blier, P. (2009). Enhancement of the function of rat serotonin and norepinephrine neurons by sustained vagus nerve stimulation. Journal of Psychiatry & Neuroscience, 34(4), 272–280.Google ScholarPubMed
Marshall, L., Mölle, M., Hallschmid, M., & Born, J. (2004). Transcranial direct current stimulation during sleep improves declarative memory. Journal of Neuroscience, 24(44), 9985–9992.CrossRefGoogle ScholarPubMed
Meinzer, M., Jähnigen, S., Copland, D. A., Darkow, R., Grittner, U., Avirame, K., Rodriguez, A. D., Lindenberg, R., & Flöel, A. (2014). Transcranial direct current stimulation over multiple days improves learning and maintenance of a novel vocabulary. Cortex, 50, 137–147.CrossRefGoogle ScholarPubMed
Miniussi, C., Cappa, S. F., Cohen, L. G., Flöel, A., Fregni, F., Nitsche, M. A., Oliveri, M., Pascuel-Leone, A., Paulus, W., Priori, A., & Walsh, V. (2008). Efficacy of repetitive transcranial magnetic stimulation/transcranial direct current stimulation in cognitive neurorehabilitation. Brain Stimulation, 1, 326–336.CrossRefGoogle ScholarPubMed
Mottaghy, F. M., Hungs, M., Brügmann, M., Sparing, R., Boroojerdi, B., Foltys, H., Huber, W., & Töpper, R. (1999). Facilitation of picture naming after repetitive transcranial magnetic stimulation. Neurology, 53(8), 1806.CrossRefGoogle ScholarPubMed
Moyer, A. (2014). Exceptional outcomes in L2 phonology: The critical factors of learner engagement and self-regulation. Applied Linguistics, 35(4), 418–440.CrossRefGoogle Scholar
Ohlenforst, B., Zekveld, A. A., Lunner, T., Wendt, D., Naylor, G., Wang, Y., Versfeld, N. J., & Kramer, S. E. (2017). Impact of stimulus-related factors and hearing impairment on listening effort as indicated by pupil dilation. Hearing Research, 351, 68–79. https://doi.org/10.1016/j.heares.2017.05.012CrossRefGoogle ScholarPubMed
Ohn, S. H., Park, C. I., Yoo, W. K., Ko, M. H., Choi, K. P., Kim, G. M., Lee, Y. T., & Kim, Y. H. (2008). Time-dependent effect of transcranial direct current stimulation on the enhancement of working memory. Neuroreport, 19(1), 43–47.CrossRefGoogle ScholarPubMed
Ollen, J. E. (2006). A criterion-related validity test of selected indicators of musical sophistication using expert ratings [Unpublished doctoral dissertation]. Ohio State University, Ohio.Google Scholar
Pascual-Leone, A., Walsh, V., & Rothwell, J. (2000). Transcranial magnetic stimulation in cognitive neuroscience–virtual lesion, chronometry, and functional connectivity. Current Opinion in Neurobiology, 10, 232–237.CrossRefGoogle Scholar
Pelzl, E. (2019). What makes second language perception of Mandarin tones hard?: A non-technical review of evidence from psycholinguistic research. Chinese as a Second Language, 54(1), 51–78.Google Scholar
Pelzl, E., Lau, E. F., Guo, T., & DeKeyser, R. (2019). Advanced second language learners’ perception of lexical tone contrasts. Studies in Second Language Acquisition, 41(1), 59–86.CrossRefGoogle Scholar
Perrachione, T. K., Lee, J., Ha, L. Y., & Wong, P. C. (2011). Learning a novel phonological contrast depends on interactions between individual differences and training paradigm design. The Journal of the Acoustical Society of America, 130(1), 461–472.CrossRefGoogle ScholarPubMed
Pichora-Fuller, M. K., Kramer, S. E., Eckert, M. A., Edwards, B., Hornsby, B. W., Humes, L. E., Lemke, U., Lunner, T., Matthen, M., Mackersie, C. L., Naylor, G., Phillips, N. A., Richter, M., Rudner, M., Sommers, M. S., & Tremblay, K. L. (2016). Hearing impairment and cognitive energy: The framework for understanding effortful listening (FUEL). Ear and Hearing, 37, 5S–27S.CrossRefGoogle Scholar
Psychology Software Tools (2012). E-Prime (Version 2.0) [Computer software]. Pittsburgh, PA.Google Scholar
R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from https://www.R-project.org/.Google Scholar
Reis, J., Robertson, E. M., Krakauer, J. W., Rothwell, J., Marshall, L., Gerloff, C., Wassermann, E. M., Pascuel-Leone, A., Hummel, F., Celnik, P. A., Classen, J., Flöel, A., Ziemann, U., Paulus, W., Siebner, H. R., Born, J., & Cohen, L. G. (2008). Consensus: Can transcranial direct current stimulation and transcranial magnetic stimulation enhance motor learning and memory formation? Brain Stimulation, 1, 363–369.CrossRefGoogle ScholarPubMed
Sakai, K. L., Noguchi, Y., Takeuchi, T., & Watanabe, E. (2002). Selective priming of syntactic processing by event-related transcranial magnetic stimulation of Broca's area. Neuron, 35(6), 1177–1182.CrossRefGoogle ScholarPubMed
Samuels, E. R., & Szabadi, E. (2008). Functional neuroanatomy of the noradrenergic locus coeruleus: Its roles in the regulation of arousal and autonomic function part I: principles of functional organisation. Current Neuropharmacology, 6(3), 235–253.CrossRefGoogle ScholarPubMed
Schmidtke, J. (2018). Pupillometry in linguistic research: An introduction and review for second language researchers. Studies in Second Language Acquisition, 40(3), 529–549.CrossRefGoogle Scholar
Sebastián-Gallés, N., & Díaz, B. (2012). First and second language speech perception: Graded learning. Language Learning, 62, 131–147.CrossRefGoogle Scholar
Sóskuthy, M. (2017). Generalised additive mixed models for dynamic analysis in linguistics: A practical introduction. arXiv preprint arXiv : 1703.05339.Google Scholar
van der Wel, P., & van Steenbergen, H. (2018). Pupil dilation as an index of effort in cognitive control tasks: A review. Psychonomic Bulletin & Review, 25(6), 2005–2015.CrossRefGoogle ScholarPubMed
van Rij, J., Hendriks, P., van Rijn, H., Baayen, R. H., & Wood, S. N. (2019). Analyzing the time course of pupillometric data. Trends in Hearing, 23, 1–23.CrossRefGoogle ScholarPubMed
Vanderwal, T., Kelly, C., Eilbott, J., Mayes, L. C., & Castellanos, F. X. (2015). Inscapes: A movie paradigm to improve compliance in functional magnetic resonance imaging. NeuroImage, 122, 222–232.CrossRefGoogle ScholarPubMed
Voeten, C. C. (2019). buildmer: Stepwise elimination and term reordering for mixed-effects regression. R package version 1.3.Google Scholar
Vonck, K., Raedt, R., Naulaerts, J., De Vogelaere, F., Thiery, E., Van Roost, D., Aldenkamp, B., Miatton, M., & Boon, P. (2014). Vagus nerve stimulation… 25 years later! What do we know about the effects on cognition? Neuroscience & Biobehavioral Reviews, 45, 63–71.CrossRefGoogle Scholar
Walsh, V., & Pascual-Leone, A. (2003). Transcranial magnetic stimulation: A neurochronometrics of mind. MIT Press.CrossRefGoogle Scholar
Wong, H. (1953). Outline of the Mandarin phonemic system. Word, 9(3), 268–276. DOI: 10.1080/00437956.1953.11659474CrossRefGoogle Scholar
Wong, P. C., & Perrachione, T. K. (2007). Learning pitch patterns in lexical identification by native English-speaking adults. Applied Psycholinguistics, 28(4), 565–585.CrossRefGoogle Scholar
Wood, S. N. (2017). Generalized additive models: An introduction with R (2nd edition). CRC Press.CrossRefGoogle Scholar
You, D. S., Kim, D.-Y., Chun, M. H., Jung, S. E., & Park, S. J. (2011). Cathodal transcranial direct current stimulation of the right Wernicke's area improves comprehension in subacute stroke patients. Brain & Language, 199, 1–5.CrossRefGoogle Scholar
Zekveld, A. A., Koelewijn, T., & Kramer, S. E. (2018). The pupil dilation response to auditory stimuli: Current state of knowledge. Trends in Hearing, 22, 1–25.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Pandža et al. supplementary material

Tables S1-S7

Download Pandža et al. supplementary material(PDF)
PDF 118 KB