Clinical Neuroscience
A novel approach for documenting naming errors induced by navigated transcranial magnetic stimulation

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Abstract

Transcranial magnetic stimulation (TMS) is widely used both in basic research and in clinical practice. TMS has been utilized in studies of functional organization of speech in healthy volunteers. Navigated TMS (nTMS) allows preoperative mapping of the motor cortex for surgical planning. Recording behavioral responses to nTMS in the speech-related cortical network in a manner that allows off-line review of performance might increase utility of nTMS both for scientific and clinical purposes, e.g., for a careful preoperative planning.

Four subjects participated in the study. The subjects named pictures of objects presented every 2-3 s on a computer screen. One-second trains of 5 pulses were applied by nTMS 300 ms after the presentation of pictures. The nTMS and stimulus presentation screens were cloned. A commercial digital camera was utilized to record the subject's performance and the screen clones. Delays between presentation, audio and video signals were eliminated by carefully tested combination of displays and camera. An experienced neuropsychologist studied the videos and classified the errors evoked by nTMS during the object naming.

Complete anomias, semantic, phonological and performance errors were observed during nTMS of left fronto-parieto-temporal cortical regions. Several errors were detected only in the video classification.

nTMS combined with synchronized video recording provides an accurate monitoring tool of behavioral TMS experiments. This experimental setup can be particularly useful for high-quality cognitive paradigms and for clinical purposes.

Highlights

► We developed a method that combines navigated TMS (nTMS) and synchronized video recording. ► The setup allows careful monitoring of the effect of nTMS on object naming. ► We present speech-related errors induced by nTMS in off-line analysis of the videos. ► This setup is useful for cognitive paradigms and for preoperative surgical planning.

Introduction

Transcranial magnetic stimulation (TMS) is widely used both in brain research and in clinical practice. TMS has been applied for studying the functional organization of speech in healthy volunteers with variable results (Pascual-Leone et al., 1991, Devlin and Watkins, 2007). For example, repetitive TMS of inferior frontal gyrus (IFG) and posterior middle temporal cortex disrupts processing of executively demanding semantic judgments (Whitney et al., 2011). However, the utilization of this information has not yet been introduced to neurosurgical planning. In navigated transcranial magnetic stimulation (nTMS) the cortical activity is elicited by magnetic pulses in cortical sites that can be defined anatomically from the individual patient's brain MRIs. The observed eloquent stimulation sites can be used for surgical planning and can be transferred into the operating room via neuronavigation. nTMS has been suggested to provide useful information in preoperative localization of motor cortex (Picht et al., 2009, Vitikainen et al., 2009). The feasibility of this approach, its superiority to fMRI analysis and also its accuracy compared with direct cortical stimulations (DCS) has been recently demonstrated for nTMS motor mapping (Forster et al., 2011, Picht et al., 2011). The activated sites in nTMS and DCS are separated by 5–10 mm; corresponding separation between DCS and fMRI is 15 mm (Forster et al., 2011). nTMS has been approved for preoperative localization of motor cortex by Food and Drug Administration of U.S.A. (K091457).

Producing and understanding speech involves an extensive network of brain areas in both hemispheres. Traditionally, the left hemisphere has been considered to be predominantly involved in producing and understanding speech whereas the right hemisphere has been suggested to process emotional and prosodic speech properties. Clinical research has emphasized the importance of the left inferior frontal gyrus. Nevertheless, e.g., impaired semantic control can also follow left temporo-parietal lesions, emphasizing again the role of large-scale cortical networks in speech processing. In direct cortical stimulation, extensive cortical variation of locations producing speech related errors has been observed throughout the frontal, parietal and temporal lobes (Pouratian and Bookheimer, 2010).

Data from several studies have demonstrated clear benefit of surgical resection and maximal cytoreduction of gliomas (Stummer and Kamp, 2009). However when tumors are in close vicinity of eloquent cortical areas, preservation of cerebral function needs to be considered in connection with maximizing the resection (Duffau, 2010), by balancing against the risk of causing or increasing neurological symptoms. Several preoperative and intraoperative methods have been suggested to be useful to produce individually meaningful maps of cortical and subcortical functionally critical areas (Gil-Robles and Duffau, 2010).

The efficacy of the stimulation of motor cortex by nTMS can be measured, analyzed and documented by recording the elicited motor evoked potentials (MEPs). This possibility is not available in studies of speech-related cortical activity by nTMS. Recording behavioral responses to nTMS in speech-related cortical areas in a manner that allows off-line review of the individual's performance could improve localization accuracy, and detection of subtle errors. Moreover, it would provide documentation of the stimulation for further review. The uncoupling of the analysis from the actual recording would provide greater flexibility for data analysis, e.g., semi blind analysis by a specialist not taking part in the actual experiment.

We propose such a setup that employs synchronous video and audio recording combined with nTMS to document individual's performance. It is useful both for studies of basic physiology and for testing the usefulness of nTMS localization utility in planning neurosurgical procedures, e.g., the placement of subdural electrodes and designing subdural stimulation sequences in the vicinity of the eloquent cortex. To the best of our knowledge, no such setup has been utilized previously in cortical nTMS mapping.

Section snippets

Subjects

To test this setup, we studied four healthy subjects (three males and one female; age range 22–55 years) having no neurological disorders. Three of them were right-handed. All of them were native speakers of Finnish. The ethical committee of the Helsinki University Central Hospital approved the experimental procedures of the study in accordance with the declaration of Helsinki. A written informed consent was obtained from all subjects.

Experimental setup

For navigated TMS we used eXimia NBS version 3.2 (Nexstim

Results

The nTMS revealed 3 sites in individual subjects where a complete anomia was elicited by the used stimulation (Fig. 2). These were the inferior frontal gyrus (IFG), the superior temporal gyrus (STG), and the supramarginal gyrus (SMG). In one subject anomia was observed in the angular gyrus. Although the variability of these sites was considerable between subjects, anomia was more reproducible in IFG (see Fig. 3). Moreover, performance errors and paraphasias were observed in SMG, IFG, STG and

Discussion

The experimental setup described here provided a high-fidelity report of the experiment testing the feasibility of nTMS in mapping speech related cortical areas. It allowed precise documentation of the effective stimulation sites to be displayed and documented e.g., in planning of surgery. Moreover, it provided possibility for a non-biased analysis of the effects of the stimulation. Although performing such an rTMS study in a strict double-blind way is impossible as the researcher hears the

Conclusions

nTMS combined with synchronized video recording provides an accurate monitoring tool of behavioral TMS experiments. It allows off-line analysis of the performance of the subjects. Due to the utilization of one camera and clone screens no jittering between image and sound can bias the analysis of the performance. This experimental setup can be particularly useful for high-quality cognitive paradigms and for clinical purposes.

Acknowledgements

Pantelis Lioumis and Niko Mäkelä were supported by grants from SalWe-SHOK and from Helsinki University Central Hospital (EVO-funding). We would like to thank Dr. Ritva Paetau for providing us with photographs used in the object naming paradigm, and Niina Vilkas for providing the custom made head tracker.

References (27)

  • C.M. Epstein et al.

    Repetitive transcranial magnetic stimulation does not replicate the Wada test

    Neurology

    (2000)
  • M.-T. Forster et al.

    Navigated transcranial magnetic stimulation and functional magnetic resonance imaging – advanced adjuncts in preoperative planning for central region tumors

    Neurosurgery

    (2011)
  • S. Gil-Robles et al.

    Surgical management of World Health Organization Grade II gliomas in eloquent areas: the necessity of preserving a margin around functional structures

    Neurosurg Focus

    (2010)
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