Cerebellar tDCS: A Novel Approach to Augment Language Treatment Post-stroke

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http://journal.frontiersin.org/article/10.3389/fnhum.2016.00695/full?

Rajani Sebastian¹, Sadhvi Saxena¹, Kyrana Tsapkini¹, Andreia V. Faria², Charltien Long¹, Amy Wright¹, Cameron Davis¹, Donna C. Tippett^1,3, Antonios P. Mourdoukoutas⁴, Marom Bikson⁴, Pablo Celnik^1,5,6 and Argye E. Hillis^1,5,7*

• ¹Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA
• ²Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, MD, USA
• ³Department of Otolaryngology—Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA
• ⁴Department of Biomedical Engineering, The City College of New York of CUNY, New York, NY, USA
• ⁵Department of Physical Medicine and Rehabilitation, Johns Hopkins University School of Medicine, Baltimore, MD, USA
• ⁶Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD, USA
• ⁷Department of Cognitive Science, Johns Hopkins University, Baltimore, MD, USA

People with post-stroke aphasia may have some degree of chronic deficit for which current rehabilitative treatments are variably effective. Accumulating evidence suggests that transcranial direct current stimulation (tDCS) may be useful for enhancing the effects of behavioral aphasia treatment. However, it remains unclear which brain regions should be stimulated to optimize effects on language recovery. Here, we report on the therapeutic potential of right cerebellar tDCS in augmenting language recovery in SMY, who sustained bilateral MCA infarct resulting in aphasia and anarthria. We investigated the effects of 15 sessions of anodal cerebellar tDCS coupled with spelling therapy using a randomized, double-blind, sham controlled within-subject crossover trial. We also investigated changes in functional connectivity using resting state functional magnetic resonance imaging before and 2 months post-treatment. Both anodal and sham treatments resulted in improved spelling to dictation for trained and untrained words immediately after and 2 months post-treatment. However, there was greater improvement with tDCS than with sham, especially for untrained words. Further, generalization to written picture naming was only noted during tDCS but not with sham. The resting state functional connectivity data indicate that improvement in spelling was accompanied by an increase in cerebro-cerebellar network connectivity. These results highlight the therapeutic potential of right cerebellar tDCS to augment spelling therapy in an individual with large bilateral chronic strokes.

Introduction

Aphasia is a leading cause of disability following stroke and can affect every aspect of daily life, including interpersonal relationships, work, and community interactions. Speech-language therapy is the mainstay of treatment. Therapy is beneficial for language recovery; however, gains in therapy are variable and progress may be slow, especially after large, chronic left hemisphere lesions (Brady et al., 2016). Recently, neuromodulation with tDCS has been introduced to increase the efficiency of speech and language therapy (for recent reviews see de Aguiar et al., 2015; Sebastian et al., 2016b). Studies indicate that anodal tDCS over peri-lesional left hemisphere (LH) language regions has the potential to augment language outcomes in individuals with chronic aphasia (e.g., Baker et al., 2010; Fiori et al., 2011; Fridriksson et al., 2011; Vestito et al., 2014). However, large LH stroke impedes improvement of language functions that are dependent on LH networks. In such cases, enhancing the function of non-damaged hemisphere with the goal of facilitating compensation has been investigated. However, some data suggest that recruitment of right hemisphere (RH) regions can be maladaptive in the chronic stage. Also, several studies have shown benefit of RH inhibitory (cathodal) tDCS or combined LH anodal tDCS + RH cathodal tDCS (e.g., Marangolo et al., 2014; Manenti et al., 2015). However, inhibition of the RH might have detrimental effects on cognitive functions that normally rely on the RH. Previous studies have not evaluated the effect of tDCS in individuals with large, bilateral chronic stroke.

This case study illustrates the potential usefulness of a novel electrode placement for tDCS augmentation of language therapy in chronic post-stroke aphasia: the right cerebellum.

Evidence from functional neuroimaging and neuroanatomical investigations indicate that the right cerebellum is important for language and cognitive functions (e.g., Leiner et al., 1989; Schmahmann, 1991, 2001; Middleton and Strick, 1994; Stoodley and Schmahmann, 2009; Murdoch, 2010; Stoodley et al., 2012; Marien et al., 2014; for recent reviews see De Smet et al., 2013; Keren-Happuch et al., 2014). Damage to the right cerebellum has been associated with deficits in a variety of language tasks (e.g., Hassid, 1995; Marien et al., 1996, 2000; Gómez Beldarrain et al., 1997; Fabbro et al., 2004; Baillieux et al., 2010). In addition, cerebellar tDCS studies in healthy individuals provide evidence that right cerebellar tDCS modulates cognitive and language functions such as verb generation (Pope and Miall, 2012), verbal fluency (Turkeltaub et al., 2016), working memory (Boehringer et al., 2013; Macher et al., 2014), and implicit learning (Ferrucci et al., 2013). See Grimaldi et al. (2016) for a recent review. Beneficial cognitive effects from right cerebellar tDCS have been found for both anodal and cathodal stimulation.

Given the role of the cognitive and language functions of the cerebellum and the ability of cerebellar tDCS to modify behavior in healthy individuals, cerebellar tDCS may have a uniquely valuable therapeutic role for individuals with aphasia. Furthermore, cerebellum can be stimulated even in patients with aphasia associated with bilateral hemispheric strokes. In addition, the cerebellum is regarded as an important region involved in skill learning (Morton and Bastian, 2006; Galea et al., 2011). Therefore, cerebellar tDCS could also augment response to language therapy by enhancing learning skills.

Here, we report behavioral and neural effects of right cerebellar tDCS with behavioral spelling treatment in a participant who sustained bilateral MCA infarct resulting in aphasia and complete anarthria. Participant SMY is mute following his second stroke but has retained some ability to write and type. Because he depends on writing to communicate, recognizable spelling is critical for effective social function. Therefore, cerebellar tDCS plus behavioral spelling treatment could improve spelling recovery through its roles in language and learning. We sought to evaluate the following hypotheses: (1) Improvement in spelling to dictation (in treated and untreated words) will be greater with tDCS + spelling treatment than with sham + spelling treatment; (2) Improvement will last longer after tDCS treatment than sham treatment at 2 months post-treatment; (3) Improvement in other language tasks (written picture naming) will be greater after tDCS than sham; (4) Functional connectivity between the right cerebellum and the residual left and right hemisphere language regions of interest will be greater post-treatment compared to pre-treatment.

Case report follows.