Task-concurrent anodal tDCS modulates bilateral plasticity in the human suprahyoid motor cortex

Shaofeng Zhao, Zulin Dou, Xiaomei Wei, Jin Li, Meng Dai, Yujue Wang, Qinglu Yang, Huai He, Shaofeng Zhao, Zulin Dou, Xiaomei Wei, Jin Li, Meng Dai, Yujue Wang, Qinglu Yang, Huai He

Abstract

Transcranial direct current stimulation (tDCS) is a non-invasive method to modulate cortical excitability in humans. Here, we examined the effects of anodal tDCS on suprahyoid motor evoked potentials (MEP) when applied over the hemisphere with stronger and weaker suprahyoid/submental projections, respectively, while study participants performed a swallowing task. Thirty healthy volunteers were invited to two experimental sessions and randomly assigned to one of two different groups. While in the first group stimulation was targeted over the hemisphere with stronger suprahyoid projections, the second group received stimulation over the weaker suprahyoid projections. tDCS was applied either as anodal or sham stimulation in a random cross-over design. Suprahyoid MEPs were assessed immediately before intervention, as well as 5, 30, 60, and 90 min after discontinuation of stimulation from both the stimulated and non-stimulated contralateral hemisphere. We found that anodal tDCS (a-tDCS) had long-lasting effects on suprahyoid MEPs on the stimulated side in both groups (tDCS targeting the stronger projections: F (1,14) = 96.2, p < 0.001; tDCS targeting the weaker projections: F (1,14) = 37.45, p < 0.001). While MEPs did not increase when elicited from the non-targeted hemisphere after stimulation of the stronger projections (F (1,14) = 0.69, p = 0.42), we found increased MEPs elicited from the non-targeted hemisphere after stimulating the weaker projections (at time points 30-90 min) (F (1,14) = 18.26, p = 0.001). We conclude that anodal tDCS has differential effects on suprahyoid MEPs elicited from the targeted and non-targeted hemisphere depending on the site of stimulation. This finding may be important for the application of a-tDCS in patients with dysphagia, for example after stroke.

Keywords: brain stimulation; dysphagia; plasticity; swallowing; task; transcranial direct current stimulation.

Figures

Figure 1
Figure 1
Flow diagram of experiment protocols showing the time points for measurements and interventions. tDCS, transcranial direct current stimulation.
Figure 2
Figure 2
tDCS over the stronger hemisphere concurrent with the swallowing task. (A) a-tDCS increased suprahyoid cortical excitability in the stronger hemisphere. (B) a-tDCS had no effects on the weaker hemisphere (*p < 0.05; **p < 0.001, compared with sham, respectively).
Figure 3
Figure 3
tDCS over the weaker hemisphere concurrent with the swallowing task. a-tDCS increases suprahyoid cortical excitability of the (A)weaker and (B) stronger hemisphere (*p < 0.05; **p < 0.001, compared with sham, respectively).
Figure 4
Figure 4
Effects of a-tDCS over bilateral neurophysiology concurrent with the swallowing task. (A) When the stronger hemisphere was targeted, a-tDCS enhanced ipsilateral, but not contralateral, suprahyoid region cortical excitability. The peak response of MEPs on the stronger hemisphere was observed at 30 min post a-tDCS. (B) When the weaker hemisphere was targeted, a-tDCS enhanced both ipsilateral and contralateral suprahyoid-region cortical excitability. The peak response of MEPs on the stronger hemisphere was observed at 90 min, while that on the weaker hemisphere was present at 60 min post a-tDCS (*p < 0.05; **p < 0.001, compared with baseline, respectively).

References

    1. Al-Toubi A. K., Abu-Hijleh A., Huckabee M. L., Macrae P., Doeltgen S. H. (2011). Effects of repeated volitional swallowing on the excitability of submental corticobulbar motor pathways. Dysphagia 26, 311–317. 10.1007/s00455-010-9313-1
    1. Babaei A., Ward B. D., Siwiec R. M., Ahmad S., Kern M., Nencka A., et al. . (2013). Functional connectivity of the cortical swallowing network in humans. Neuroimage 76, 33–44. 10.1016/j.neuroimage.2013.01.037
    1. Bloom J. S., Hynd G. W. (2005). The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychol. Rev. 15, 59–71. 10.1007/s11065-005-6252-y
    1. Bradnam L. V., Stinear C. M., Lewis G. N., Byblow W. D. (2010). Task-dependent modulation of inputs to proximal upper limb following transcranial direct current stimulation of primary motor cortex. J. Neurophysiol. 103, 2382–2389. 10.1152/jn.01046.2009
    1. Brunoni A. R., Nitsche M. A., Bolognini N., Bikson M., Wagner T., Merabet L., et al. . (2012). Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul. 5, 175–195. 10.1016/j.brs.2011.03.002
    1. Chrysikou E. G., Hamilton R. H. (2011). Noninvasive brain stimulation in the treatment of aphasia: exploring interhemispheric relationships and their implications for neurorehabilitation. Restor. Neurol. Neurosci. 29, 375–394. 10.3233/RNN-2011-0610
    1. Cosentino G., Alfonsi E., Brighina F., Fresia M., Fierro B., Sandrini G., et al. . (2014). Transcranial direct current stimulation enhances sucking of a liquid bolus in healthy humans. Brain Stimul. 7, 817–822. 10.1016/j.brs.2014.09.007
    1. Daniels S. K., Corey D. M., Fraychinaud A., DePolo A., Foundas A. L. (2006). Swallowing lateralization: the effects of modified dual-task interference. Dysphagia 21, 21–27. 10.1007/s00455-005-9007-2
    1. Daskalakis Z. J., Christensen B. K., Fitzgerald P. B., Roshan L., Chen R. (2002). The mechanisms of interhemispheric inhibition in the human motor cortex. J. Physiol. 543, 317–326. 10.1113/jphysiol.2002.017673
    1. Doeltgen S. H., Ridding M. C., O’beirne G. A., Dalrymple-Alford J., Huckabee M. L. (2009). Test-retest reliability of motor evoked potentials (MEPs) at the submental muscle group during volitional swallowing. J. Neurosci. Methods 178, 134–137. 10.1016/j.jneumeth.2008.12.005
    1. Ferbert A., Priori A., Rothwell J. C., Day B. L., Colebatch J. G., Marsden C. D. (1992). Interhemispheric inhibition of the human motor cortex. J. Physiol. 453, 525–546. 10.1113/jphysiol.1992.sp019243
    1. Filmer H. L., Dux P. E., Mattingley J. B. (2014). Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci. 37, 742–753. 10.1016/j.tins.2014.08.003
    1. Flöel A. (2014). tDCS-enhanced motor and cognitive function in neurological diseases. Neuroimage 85, 934–947. 10.1016/j.neuroimage.2013.05.098
    1. Fritsch B., Reis J., Martinowich K., Schambra H. M., Ji Y., Cohen L. G., et al. . (2010). Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66, 198–204. 10.1016/j.neuron.2010.03.035
    1. Gallas S., Marie J. P., Leroi A. M., Verin E. (2009). Impact of swallowing and ventilation on oropharyngeal cortical representation. Respir. Physiol. Neurobiol. 167, 208–213. 10.1016/j.resp.2009.04.022
    1. Gandiga P. C., Hummel F. C., Cohen L. G. (2006). Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin. Neurophysiol. 117, 845–850. 10.1016/j.clinph.2005.12.003
    1. Gentner R., Wankerl K., Reinsberger C., Zeller D., Classen J. (2008). Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb. Cortex 18, 2046–2053. 10.1093/cercor/bhm239
    1. Gow D., Rothwell J., Hobson A., Thompson D., Hamdy S. (2004). Induction of long-term plasticity in human swallowing motor cortex following repetitive cortical stimulation. Clin. Neurophysiol. 115, 1044–1051. 10.1016/j.clinph.2003.12.001
    1. Hamdy S., Aziz Q., Rothwell J. C., Crone R., Hughes D., Tallis R. C., et al. . (1997). Explaining oropharyngeal dysphagia after unilateral hemispheric stroke. Lancet 350, 686–692. 10.1016/s0140-6736(97)02068-0
    1. Hamdy S., Aziz Q., Rothwell J. C., Power M., Singh K. D., Nicholson D. A., et al. . (1998). Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex. Gastroenterology 115, 1104–1112. 10.1016/s0016-5085(98)70081-2
    1. Hamdy S., Rothwell J. C., Aziz Q., Thompson D. G. (2000). Organization and reorganization of human swallowing motor cortex: implications for recovery after stroke. Clin. Sci. (Lond) 99, 151–157. 10.1042/cs19990300
    1. Hummel F., Celnik P., Giraux P., Floel A., Wu W. H., Gerloff C., et al. . (2005). Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128, 490–499. 10.1093/brain/awh369
    1. Jean A. (2001). Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol. Rev. 81, 929–969.
    1. Jefferson S., Mistry S., Singh S., Rothwell J., Hamdy S. (2009). Characterizing the application of transcranial direct current stimulation in human pharyngeal motor cortex. Am. J. Physiol. Gastrointest. Liver Physiol. 297, G1035–G1040. 10.1152/ajpgi.00294.2009
    1. Kessler S. K., Turkeltaub P. E., Benson J. G., Hamilton R. H. (2012). Differences in the experience of active and sham transcranial direct current stimulation. Brain Stimul. 5, 155–162. 10.1016/j.brs.2011.02.007
    1. Kumar S., Wagner C. W., Frayne C., Zhu L., Selim M., Feng W., et al. . (2011). Noninvasive brain stimulation may improve stroke-related dysphagia: a pilot study. Stroke 42, 1035–1040. 10.1161/STROKEAHA.110.602128
    1. Leopold N. A., Daniels S. K. (2010). Supranuclear Control of Swallowing. Dysphagia 25, 250–257. 10.1007/s00455-009-9249-5
    1. Liew S. L., Santarnecchi E., Buch E. R., Cohen L. G. (2014). Non-invasive brain stimulation in neurorehabilitation: local and distant effects for motor recovery. Front Hum Neurosci 8:378. 10.3389/fnhum.2014.00378
    1. Lowell S. Y., Reynolds R. C., Chen G., Horwitz B., Ludlow C. L. (2012). Functional connectivity and laterality of the motor and sensory components in the volitional swallowing network. Exp. Brain Res. 219, 85–96. 10.1007/s00221-012-3069-9
    1. Meyer B. U., Röricht S., Woiciechowsky C. (1998). Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices. Ann. Neurol. 43, 360–369. 10.1002/ana.410430314
    1. Michou E., Hamdy S. (2009). Cortical input in control of swallowing. Curr. Opin. Otolaryngol. Head Neck Surg. 17, 166–171. 10.1097/MOO.0b013e32832b255e
    1. Mistry S., Michou E., Rothwell J., Hamdy S. (2012). Remote effects of intermittent theta burst stimulation of the human pharyngeal motor system. Eur. J. Neurosci. 36, 2493–2499. 10.1111/j.1460-9568.2012.08157.x
    1. Mistry S., Verin E., Singh S., Jefferson S., Rothwell J. C., Thompson D. G., et al. . (2007). Unilateral suppression of pharyngeal motor cortex to repetitive transcranial magnetic stimulation reveals functional asymmetry in the hemispheric projections to human swallowing. J. Physiol. 585, 525–538. 10.1113/jphysiol.2007.144592
    1. Murase N., Duque J., Mazzocchio R., Cohen L. G. (2004). Influence of interhemispheric interactions on motor function in chronic stroke. Ann. Neurol. 55, 400–409. 10.1002/ana.10848
    1. Nitsche M. A., Fricke K., Henschke U., Schlitterlau A., Liebetanz D., Lang N., et al. . (2003). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J. Physiol. 553, 293–301. 10.1113/jphysiol.2003.049916
    1. Nitsche M. A., Paulus W. (2001). Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57, 1899–1901. 10.1212/wnl.57.10.1899
    1. Oldfield R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113. 10.1016/0028-3932(71)90067-4
    1. Olma M. C., Dargie R. A., Behrens J. R., Kraft A., Irlbacher K., Fahle M., et al. . (2013). Long-Term Effects of Serial Anodal tDCS on Motion Perception in Subjects with Occipital Stroke Measured in the Unaffected Visual Hemifield. Front Hum Neurosci 7:314. 10.3389/fnhum.2013.00314
    1. Pellicciari M. C., Brignani D., Miniussi C. (2013). Excitability modulation of the motor system induced by transcranial direct current stimulation: a multimodal approach. Neuroimage 83, 569–580. 10.1016/j.neuroimage.2013.06.076
    1. Perez M. A., Lungholt B. K. S., Nyborg K., Nielsen J. B. (2004). Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp. Brain Res. 159, 197–205. 10.1007/s00221-004-1947-5
    1. Plowman-Prine E. K., Triggs W. J., Malcolm M. P., Rosenbek J. C. (2008). Reliability of transcranial magnetic stimulation for mapping swallowing musculature in the human motor cortex. Clin. Neurophysiol. 119, 2298–2303. 10.1016/j.clinph.2008.06.006
    1. Polanía R., Nitsche M. A., Paulus W. (2011a). Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation. Hum. Brain Mapp. 32, 1236–1249. 10.1002/hbm.21104
    1. Polanía R., Paulus W., Antal A., Nitsche M. A. (2011b). Introducing graph theory to track for neuroplastic alterations in the resting human brain: a transcranial direct current stimulation study. Neuroimage 54, 2287–2296. 10.1016/j.neuroimage.2010.09.085
    1. Polanía R., Paulus W., Nitsche M. A. (2012). Modulating cortico-striatal and thalamo-cortical functional connectivity with transcranial direct current stimulation. Hum. Brain Mapp. 33, 2499–2508. 10.1002/hbm.21380
    1. Shigematsu T., Fujishima I., Ohno K. (2013). Transcranial direct current stimulation improves swallowing function in stroke patients. Neurorehabil. Neural Repair 27, 363–369. 10.1177/1545968312474116
    1. Silvanto J., Muggleton N., Lavie N., Walsh V. (2009). The perceptual and functional consequences of parietal top-down modulation on the visual cortex. Cereb. Cortex 19, 327–330. 10.1093/cercor/bhn091
    1. Sörös P., Inamoto Y., Martin R. E. (2009). Functional brain imaging of swallowing: an activation likelihood estimation meta-analysis. Hum. Brain Mapp. 30, 2426–2439. 10.1002/hbm.20680
    1. Stagg C. J., Lin R. L., Mezue M., Segerdahl A., Kong Y., Xie J., et al. . (2013). Widespread modulation of cerebral perfusion induced during and after transcranial direct current stimulation applied to the left dorsolateral prefrontal cortex. J. Neurosci. 33, 11425–11431. 10.1523/JNEUROSCI.3887-12.2013
    1. Suntrup S., Teismann I., Wollbrink A., Winkels M., Warnecke T., Flöel A., et al. . (2013). Magnetoencephalographic evidence for the modulation of cortical swallowing processing by transcranial direct current stimulation. Neuroimage 83, 346–354. 10.1016/j.neuroimage.2013.06.055
    1. Teismann I. K., Dziewas R., Steinstraeter O., Pantev C. (2009). Time-dependent hemispheric shift of the cortical control of volitional swallowing. Hum. Brain Mapp. 30, 92–100. 10.1002/hbm.20488
    1. Vasant D. H., Mistry S., Michou E., Jefferson S., Rothwell J. C., Hamdy S. (2014). Transcranial direct current stimulation reverses neurophysiological and behavioural effects of focal inhibition of human pharyngeal motor cortex on swallowing. J. Physiol. 592, 695–709. 10.1113/jphysiol.2013.263475
    1. Yang E. J., Baek S. R., Shin J., Lim J. Y., Jang H. J., Kim Y. K., et al. . (2012). Effects of transcranial direct current stimulation (tDCS) on post-stroke dysphagia. Restor. Neurol. Neurosci. 30, 303–311. 10.3233/RNN-2012-110213

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅