Testing the therapeutic effects of transcranial direct current stimulation (tDCS) in semantic dementia: a double blind, sham controlled, randomized clinical trial

Clara Sanches, Richard Levy, Sarah Benisty, Lisette Volpe-Gillot, Marie-Odile Habert, Aurelie Kas, Sébastian Ströer, Nadya Pyatigorskaya, Anna Kaglik, Angelina Bourbon, Bruno Dubois, Raffaella Migliaccio, Antoni Valero-Cabré, Marc Teichmann, Clara Sanches, Richard Levy, Sarah Benisty, Lisette Volpe-Gillot, Marie-Odile Habert, Aurelie Kas, Sébastian Ströer, Nadya Pyatigorskaya, Anna Kaglik, Angelina Bourbon, Bruno Dubois, Raffaella Migliaccio, Antoni Valero-Cabré, Marc Teichmann

Abstract

Background: Semantic dementia is a neurodegenerative disease that primarily affects the left anterior temporal lobe, resulting in a gradual loss of conceptual knowledge. There is currently no validated treatment. Transcranial stimulation has provided evidence for long-lasting language effects presumably linked to stimulation-induced neuroplasticity in post-stroke aphasia. However, studies evaluating its effects in neurodegenerative diseases such as semantic dementia are still rare and evidence from double-blind, prospective, therapeutic trials is required.

Objective: The primary objective of the present clinical trial (STIM-SD) is to evaluate the therapeutic efficacy of a multiday transcranial direct current stimulation (tDCS) regime on language impairment in patients with semantic dementia. The study also explores the time course of potential tDCS-driven improvements and uses imaging biomarkers that could reflect stimulation-induced neuroplasticity.

Methods: This is a double-blind, sham-controlled, randomized study using transcranial Direct Current Stimulation (tDCS) applied daily for 10 days, and language/semantic and imaging assessments at four time points: baseline, 3 days, 2 weeks and 4 months after 10 stimulation sessions. Language/semantic assessments will be carried out at these same 4 time points. Fluorodeoxyglucose positron emission tomography (FDG-PET), resting-state functional magnetic resonance imaging (rs-fMRI), T1-weighted images and white matter diffusion tensor imaging (DTI) will be applied at baseline and at the 2-week time point. According to the principle of inter-hemispheric inhibition between left (language-related) and right homotopic regions we will use two stimulation modalities - left-anodal and right-cathodal tDCS over the anterior temporal lobes. Accordingly, the patient population (n = 60) will be subdivided into three subgroups: left-anodal tDCS (n = 20), right-cathodal tDCS (n = 20) and sham tDCS (n = 20). The stimulation will be sustained for 20 min at an intensity of 1.59 mA. It will be delivered through 25cm2-round stimulation electrodes (current density of 0.06 mA/cm2) placed over the left and right anterior temporal lobes for anodal and cathodal stimulation, respectively. A group of healthy participants (n = 20) matched by age, gender and education will also be recruited and tested to provide normative values for the language/semantic tasks and imaging measures.

Discussion: The aim of this study is to assess the efficacy of tDCS for language/semantic disorders in semantic dementia. A potential treatment would be easily applicable, inexpensive, and renewable when therapeutic effects disappear due to disease progression.

Trial registration: ClinicalTrials.gov NCT03481933. Registered on March 2018.

Keywords: Language impairments; Neurodegenerative diseases; Neurology; Non-invasive brain stimulation; Primary progressive aphasia; Semantic dementia; Transcranial direct current stimulation.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
a Flow diagram from patients’ selection to the end of their participation in the study. tDCS, transcranial direct current stimulation; MRI, magnetic resonance imaging; PET, positron emission tomography; EEG, electroencephalography. b Standard protocol items: recommendations for Interventional Trials (Additional file 1). Table defining the different evaluations or interventions (left column) that would be performed for each study period or time point (top rows)
Fig. 2
Fig. 2
The three upper panels show, respectively, a coronal, b axial and c sagittal sections from magnetic resonance imaging (MRI) in a representative patient with semantic dementia (SD). The crosshair signals the location of the stimulation target in the left Anterior Temporal Lobe (ATL). d MRI-based frameless stereotactic navigation system device (Brainsight) employed for accurate targeting of the left ATL in SD patients. 3D brain curvilinear e cortical and f skin reconstructions from the MRI of a patient, provided by the neuronavigation system with a sphere indicating the left ATL target aimed by the stimulation
Fig. 3
Fig. 3
Two trials of the semantic association (SA) test in their verbal and picture modalities. a Trial with living items for the verbal modality (chenille (caterpillar) - target item, scarabée (beetle) - distractor, papillon (butterfly) - test item). b Trial with living items for the picture modality using the same items in a picture format. c Trial with non-living items for the verbal modality (ceinture (belt) - target item, pantalon (trousers) - test item, gilet (vest) - distractor). d Trial with non-living items for the picture modality using the same items in a picture format. For each trial in each modality subjects have to decide, by pressing one of two buttons in the response box, which of the items presented on the bottom of the screen is associated with the target item, on the top of the screen
Fig. 4
Fig. 4
Two illustrative trials of the executive function (EXE) task. a Trial in the verbal modality. For each trial participants have to decide which of the test items presented on the bottom of the screen begins and ends with the same letter as the target item (abeille (bee) - target item, abysse (abyss) - test item, abri (shelter) - distractor). b Trial in the picture modality. For each trial subjects have to decide which of the test items on the bottom of the screen has the same color or the same geometric form as the target item
Fig. 5
Fig. 5
Example of a computational model produced with the open-source tool ROAST for the simulation of transcranial direct current stimulation (tDCS) current magnitude and distribution using a 3D T1-weighted image from a representative SD patient. a Illustration of the montage for the left-anodal stimulation. The round blue patch represents the cathode, placed over the right supra-orbital region [10–20 electroencephalography (EEG) coordinates AF8], and the red round patch represents the anode, placed over the left Anterior Temporal Lobe (ATL) (Montreal Neurological Institute (MNI) coordinates: x = − 52, y = 2, z = − 28). b Coronal slice view of the electric field with current flow direction represented by the black arrows. c Electric field distribution on the cortical surface - right hemisphere view, left hemisphere view, upper view and frontal view. The color-bar represents the magnitude of the electric field, in Volts per meter, in different regions of the brain (for panels b and c)

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