Speech facilitation by left inferior frontal cortex stimulation

Rachel Holland, Alex P Leff, Oliver Josephs, Joseph M Galea, Mahalekshmi Desikan, Cathy J Price, John C Rothwell, Jennifer Crinion, Rachel Holland, Alex P Leff, Oliver Josephs, Joseph M Galea, Mahalekshmi Desikan, Cathy J Price, John C Rothwell, Jennifer Crinion

Abstract

Electrophysiological studies in humans and animals suggest that noninvasive neurostimulation methods such as transcranial direct current stimulation (tDCS) can elicit long-lasting [1], polarity-dependent [2] changes in neocortical excitability. Application of tDCS can have significant and selective behavioral consequences that are associated with the cortical location of the stimulation electrodes and the task engaged during stimulation [3-8]. However, the mechanism by which tDCS affects human behavior is unclear. Recently, functional magnetic resonance imaging (fMRI) has been used to determine the spatial topography of tDCS effects [9-13], but no behavioral data were collected during stimulation. The present study is unique in this regard, in that both neural and behavioral responses were recorded using a novel combination of left frontal anodal tDCS during an overt picture-naming fMRI study. We found that tDCS had significant behavioral and regionally specific neural facilitation effects. Furthermore, faster naming responses correlated with decreased blood oxygen level-dependent (BOLD) signal in Broca's area. Our data support the importance of Broca's area within the normal naming network and as such indicate that Broca's area may be a suitable candidate site for tDCS in neurorehabilitation of anomic patients, whose brain damage spares this region.

Copyright © 2011 Elsevier Ltd. All rights reserved.

Figures

Figure 1
Figure 1
Behavioral Effects of Anodal Transcranial Direct Current Stimulation Main effects of order, i.e., position of run during scanning session (P1 versus P2; A), cue (noise versus word; B), and stimulation (sham versus anodal tDCS [A-tDCS]; C), on naming reaction times (n = 10). Black bars are the control stimuli. Error bars indicate standard error of the mean (SEM). ∗∗∗p < 0.001, ∗∗p < 0.05.
Figure 2
Figure 2
Neural Effects of Anodal Transcranial Direct Current Stimulation (Ai and Aii) Statistical parametric maps showing the greatest reduction in BOLD (orange, peak; yellow, cluster) in inferior frontal sulcus (IFS; z score 4.98; Ai) and ventral premotor cortex (z score 4.62; Aii) as a consequence of A-tDCS. Effects of A-tDCS persist in left IFS peak (z score 4.62) and ventral premotor cortex peak (z score 3.67) when masked exclusively by order effects. (B–D) Mean beta value with SEM of each condition in IFS peak voxel (−48, 32, 19; B) illustrating decreased BOLD response associated with A-tDCS, and in left precentral gyrus (−36, −4, 37; C) and left anterior insula (−27, 32, 7; D) illustrating no effect of A-tDCS. Black bars are the control stimuli. All coordinates are in Montreal Neurological Institute space (x, y, z). See also Figures S1 and S2.
Figure 3
Figure 3
Relationship between Neural and Behavioral Effects Plots of neural effect size and correlations with naming reaction-time data for word- and noise-cued items in inferior frontal sulcus (A) and ventral premotor regions (B) affected by A-tDCS. Left panel reflects mean beta value and SEM for both significant peaks within the vicinity of left Broca's area. Scatter plots at center and right illustrate the spread and relationship between reaction time and activity in each region during sham P1 and anodal P1 conditions. Statistical analyses demonstrated a weak positive correlation in IFS between beta values and reaction time for word cues (r = 0.51, n = 10, p = 0.07, R2 = 0.26) but not noise control cues (r = 0.23, n = 10, p = 0.26). These correlations are shown in the top pair of scatter plots (left, word-cued effects; right, noise-cued effects). The bottom pair of scatter plots illustrate a significant correlation in ventral premotor cortex for word (left; r = 0.56, n = 10, p = 0.05, R2 = 0.32) and noise control cues (right; r = 0.66, n = 10, p = 0.02, R2 = 0.44, all one-tailed). Note the different scales on the y axes of the scatter plots. Anodal P1 and anodal P2 refer to the run order when A-tDCS was delivered within a scanning session. Black bars are the control stimuli.

References

    1. Fritsch B., Reis J., Martinowich K., Schambra H.M., Ji Y., Cohen L.G., Lu B. Direct current stimulation promotes BDNF-dependent synaptic plasticity: Potential implications for motor learning. Neuron. 2010;66:198–204.
    1. Nitsche M.A., Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 2000;527:633–639.
    1. de Vries M.H., Barth A.C.R., Maiworm S., Knecht S., Zwitserlood P., Flöel A. Electrical stimulation of Broca's area enhances implicit learning of an artificial grammar. J. Cogn. Neurosci. 2010;22:2427–2436.
    1. Flöel A., Rösser N., Michka O., Knecht S., Breitenstein C. Noninvasive brain stimulation improves language learning. J. Cogn. Neurosci. 2008;20:1415–1422.
    1. Sparing R., Dafotakis M., Meister I.G., Thirugnanasambandam N., Fink G.R. Enhancing language performance with non-invasive brain stimulation—a transcranial direct current stimulation study in healthy humans. Neuropsychologia. 2008;46:261–268.
    1. Baker J.M., Rorden C., Fridriksson J. Using transcranial direct-current stimulation to treat stroke patients with aphasia. Stroke. 2010;41:1229–1236.
    1. Fertonani A., Rosini S., Cotelli M., Rossini P.M., Miniussi C. Naming facilitation induced by transcranial direct current stimulation. Behav. Brain Res. 2010;208:311–318.
    1. Fiori V., Coccia M., Marinelli C.V., Vecchi V., Bonifazi S., Ceravolo M.G., Provinciali L., Tomaiuolo F., Marangolo P. Transcranial direct current stimulation improves word retrieval in healthy and nonfluent aphasic subjects. J. Cogn. Neurosci. 2011;23:2309–2323.
    1. Stagg C.J., O'Shea J., Kincses Z.T., Woolrich M., Matthews P.M., Johansen-Berg H. Modulation of movement-associated cortical activation by transcranial direct current stimulation. Eur. J. Neurosci. 2009;30:1412–1423.
    1. Kwon Y.H., Ko M.H., Ahn S.H., Kim Y.H., Song J.C., Lee C.H., Chang M.C., Jang S.H. Primary motor cortex activation by transcranial direct current stimulation in the human brain. Neurosci. Lett. 2008;435:56–59.
    1. Kwon Y.H., Jang S.H. The enhanced cortical activation induced by transcranial direct current stimulation during hand movements. Neurosci. Lett. 2011;492:105–108.
    1. Antal A., Polania R., Schmidt-Samoa C., Dechent P., Paulus W. Transcranial direct current stimulation over the primary motor cortex during fMRI. Neuroimage. 2011;55:590–596.
    1. Polanía R., Paulus W., Antal A., Nitsche M.A. Introducing graph theory to track for neuroplastic alterations in the resting human brain: A transcranial direct current stimulation study. Neuroimage. 2011;54:2287–2296.
    1. Crinion J.T., Leff A.P. Recovery and treatment of aphasia after stroke: Functional imaging studies. Curr. Opin. Neurol. 2007;20:667–673.
    1. Crosson B., McGregor K., Gopinath K.S., Conway T.W., Benjamin M., Chang Y.L., Moore A.B., Raymer A.M., Briggs R.W., Sherod M.G. Functional MRI of language in aphasia: A review of the literature and the methodological challenges. Neuropsychol. Rev. 2007;17:157–177.
    1. Postman-Caucheteux W.A., Birn R.M., Pursley R.H., Butman J.A., Solomon J.M., Picchioni D., McArdle J., Braun A.R. Single-trial fMRI shows contralesional activity linked to overt naming errors in chronic aphasic patients. J. Cogn. Neurosci. 2010;22:1299–1318.
    1. Fridriksson J., Bonilha L., Baker J.M., Moser D., Rorden C. Activity in preserved left hemisphere regions predicts anomia severity in aphasia. Cereb. Cortex. 2010;20:1013–1019.
    1. Iyer M.B., Mattu U., Grafman J., Lomarev M., Sato S., Wassermann E.M. Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology. 2005;64:872–875.
    1. Starreveld P.A. On the interpretation of onsets of auditory context effects in word production. J. Mem. Lang. 2000;42:497–525.
    1. de Zubicaray G.I., McMahon K.L. Auditory context effects in picture naming investigated with event-related fMRI. Cogn. Affect. Behav. Neurosci. 2009;9:260–269.
    1. Lang N., Siebner H.R., Ward N.S., Lee L., Nitsche M.A., Paulus W., Rothwell J.C., Lemon R.N., Frackowiak R.S. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur. J. Neurosci. 2005;22:495–504.
    1. Schnur T.T., Schwartz M.F., Kimberg D.Y., Hirshorn E., Coslett H.B., Thompson-Schill S.L. Localizing interference during naming: Convergent neuroimaging and neuropsychological evidence for the function of Broca's area. Proc. Natl. Acad. Sci. USA. 2009;106:322–327.
    1. Kuo M.F., Unger M., Liebetanz D., Lang N., Tergau F., Paulus W., Nitsche M.A. Limited impact of homeostatic plasticity on motor learning in humans. Neuropsychologia. 2008;46:2122–2128.

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