Introducing navigated transcranial magnetic stimulation as a refined brain mapping methodology

A major intrinsic limitation of transcranial magnetic stimulation (TMS) to map the human brain lies in the unclear relationship between the position of the stimulating coil on the scalp and the underlying stimulated cortex. The relationship between structure and function as the major feature constituting a brain mapping modality can therefore not be established. Recent advances in image processing allowed us to refine TMS by combining magnetic resonance imaging (MRI) modalities with TMS using a neuronavigation system to measure the position of the stimulating coil and map this position onto a MRI data set. This technique has several advantages over recent TMS mapping strategies. The position of the coil on the scalp can be held constant as verified by real time visual guidance. When evaluating higher cortical functions, the relationship between underlying cortical anatomy and the scalp stimulation site can be accurately assessed. Cortical motor output maps can be easily obtained for preoperative planning and decision making for mass lesions near rolandic cortex in patients. In conclusion, navigated TMS is a reliable alternative for localizing cortical functions and therefore may be a useful adjunct or in selected patients even a helpful alternative to other functional neuroimaging methods. Electronic Publication     

Functional brain mapping of patients with arteriovenous malformations using navigated transcranial magnetic stimulation: first experience in ten patients

Background

Intracranial arteriovenous malformations (AVM) are known to be potent inductors of functional plasticity, and their vasculature makes standard functional imaging difficult. Here we conducted functional mapping of both primary motor cortex and speech related areas in patients with AVM using navigated transcranial magnetic stimulation (nTMS), which has been recently proven as a reliable noninvasive modality of preoperative functional brain mapping.

Method

nTMS mapping was performed in ten patients with unruptured intracranial AVMs located in or near eloquent areas. Motor mapping was conducted for six patients with AVMs near the rolandic region, and speech mapping was performed for four patients with left perisylvian AVMs. After the examination, all patients were treated with surgery, radiosurgery or observed with best medical treatment on case-by-case basis.

Results

Motor mapping allowed for delineation of the primary motor cortex, even if the anatomy was severely obscured by the AVM in all cases with rolandic AVMs. No plastic relocation of the primary motor cortex was observed. Repetitive stimulation of the left ventral precentral gyrus led to speech impairments in all four cases that underwent speech mapping. Right hemispheric involvement was observed in one out of four cases and potentially indicated plastic changes. No side effects were observed.

Conclusion

nTMS allowed for detailed delineation of eloquent areas even within hypervascularized cortical areas. Our observations indicate that nTMS functional mapping is feasible not only in tumorous brain lesions, but also in AVMs.     

Comparison of navigated transcranial magnetic stimulation and functional magnetic resonance imaging for preoperative mapping in rolandic tumor surgery

Navigated transcranial magnetic stimulation (nTMS) is a novel tool for preoperative functional mapping. It detects eloquent cortical areas directly, comparable to intraoperative direct cortical stimulation (DCS). The aim of this study was to evaluate the advantage of nTMS in comparison with functional magnetic resonance imaging (fMRI) in the clinical setting. Special focus was placed on accuracy of motor cortex localization in patients with rolandic lesions. Thirty consecutive patients were enrolled in the study. All patients received an fMRI and nTMS examination preoperatively. Feasibility of the technique and spatial resolution of upper and lower extremity cortical mapping were compared with fMRI. Consistency of preoperative mapping with intraoperative DCS was assessed via the neuronavigation system. nTMS was feasible in all 30 patients. fMRI was impossible in 7 out of 30 patients with special clinical conditions, pediatric patients, central vascular lesions, or compliance issues. The mean accuracy to localize motor cortex of nTMS was higher than in fMRI. In the subgroup of intrinsic tumors, nTMS produced statistically significant higher accuracy scores of the lower extremity localization than fMRI. fMRI failed to localize hand or leg areas in 6 out of 23 cases. Using nTMS, a preoperative localization of the central sulcus was possible in all patients. Verification of nTMS motor cortex localization with DCS was achieved in all cases. The fMRI localization of the hand area proved to be postcentral in one case. nTMS has fewer restrictions for preoperative functional mapping than fMRI and requires only a limited level of compliance. nTMS scores higher on the accuracy scale than fMRI. nTMS represents a highly valuable supplement for the preoperative functional planning in the clinical routine.     

Brain mapping using transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) is a novel brain stimulation technique that has advanced the understanding of brain physiology, and has diagnostic value as well as therapeutic potential for several neuropsychiatric disorders. The stimulation involves restricted cortical and subcortical regions, and, when used in combination with a visually guided technique, results in improved accuracy to target specific areas, which may also influence the outcome desired. This article reviews the principles underlying the mechanism of action of TMS, and discusses its use to obtain functional maps of the motor and visual cortex, including technical considerations for accuracy and reproducibility of mapping procedures.     

The reliability of topographic measurements from navigated transcranial magnetic stimulation in healthy volunteers and tumor patients

Background

Navigated transcranial magnetic stimulation (nTMS) is increasingly being used for preoperative mapping of the motor cortex. Any new technology should undergo rigorous validation before being widely adopted in routine clinical practice. The aim of this experimental study was to assess the intraexaminer and interexaminer reliability of topographic mapping with nTMS.

Methods

nTMS mapping of the motor cortex for the first dorsal interosseous (FDI) muscle was performed by an expert and a novice examiner, twice in ten healthy volunteers and once in ten tumor patients. The distances between the centers-of-gravity and hotspots were calculated, as were coefficients of variation. This study also compared orthogonal versus variable orientation of the stimulation coil.

Results

The mean (range) distance between centers-of-gravity for the expert examiner in the test–retest protocol with healthy volunteers was 4.40 (1.86–7.68) mm. The mean (range) distance between centers-of-gravity for the expert vs. novice examiner was 4.89 (2.39–9.22) mm. There were no significant differences in this result between healthy volunteers and tumor patients.

Conclusions

nTMS is sufficiently reliable for clinical use, but examiners should make efforts to minimize sources of error. The reliability of nTMS in tumor patients appears comparable to healthy subjects.     

The interaction of brain regions during visual search processing as revealed by transcranial magnetic stimulation

Although it has long been known that right posterior parietal cortex (PPC) has a role in certain visual search tasks, and human motion area V5 is involved in processing tasks requiring attention to motion, little is known about how these areas may interact during the processing of a task requiring the speciality of each. Using transcranial magnetic stimulation (TMS), this study first established the specialization of each area in the form of a double dissociation; TMS to right PPC disrupted processing of a color/form conjunction and TMS to V5 disrupted processing of a motion/form conjunction. The key finding of this study is, however, if TMS is used to disrupt processing of V5 at its critical time of activation during the motion/form conjunction task, concurrent disruption of right PPC now has a significant effect, where TMS at PPC alone does not. Our findings challenge the conventional interpretation of the role of right PPC in conjunction search and spatial attention.     

Presurgical mapping with functional MRI: comparative study with transcranial magnetic stimulation and intraoperative mapping]

PURPOSE: The accuracy of preoperative mappings in patients with brain tumors near the central sulcus using functional magnetic resonance imaging (fMRI) or transcranical magnetic stimulation (TCS) was evaluated by comparative reference to intraoperative mapping. METHODS: The thumb movement was evoked by TCS for the mapping of the motor cortex. After the placement of the marker determined by TCS on the scalp, fMRI under motor tasks consisting of repetitive grasping was performed. For motor cortex activation, an axial oblique plane to maximize gray matter sampling in the rolandic cortex was employed in order to compare these different mapping techniques more precisely. Sixteen patients with brain tumors were included in this study. RESULTS: In nine patients, fMRI disclosed activation in one restricted gyrus or in the localized area around one restricted sulcus. Of these nine patients, preoperative TCS mapping corresponded closely with fMRI in six, while in the remaining three, the TCS marker fell between 1 and 2 cm apart from the fMRI-activated area. However, in these three patients, intraoperative electrocortical stimulation corresponded with the preoperative mapping with fMRI. In six patients, contigucus two gyri were activated by motor tasks. The TCS marker was disclosed on one of the two activated gyri. Of these six patients, the position of the TCS marker and fMRI-activated site corresponded with each other in four cases. They were found on the same gyrus but there was 1.0-2.0 cm distance between them in two cases. Intraoperative somatosensory evoked potential was monitored in two of these six cases. They corresponded well with the mapping by fMRI and TCS together. In only one patient, no significant activation area was obtained by fMRI because of excessive head motion during motor tasks. The TCS marker in this patient was identical with intraoperative electro-cortical stimulation mapping. CONCLUSION: For presurgical planning in patients with brain tumor near the central sulcus, comparative evaluation with fMRI and TCS is applicable and provides accurate functional mapping.     

The preoperative use of navigated transcranial magnetic stimulation facilitates early resection of suspected low-grade gliomas in the motor cortex

Background

Resection is recommended for low-grade gliomas, but often it is not performed if the tumor is suspected of invading the primary motor cortex. The study aim is to assess what influence preoperative navigated transcranial magnetic stimulation (nTMS) has on the treatment strategy and clinical outcome for suspected low-grade gliomas in presumed motor eloquent location.

Methods

This paper reports on all our patients with gliomas in the primary motor cortex that were non-enhancing on MRI, since we began using nTMS (n?=?11). For the comparison group, we identified the 11 most recent such patients just before we started using nTMS.

Results

Exact delineation of motor functional versus non-functional cortical tissue was provided by nTMS in all cases, also within the area of altered FLAIR signal. In 6 out of 11 cases, the nTMS mapping result changed the treatment plan towards early and more extensive resection. Only one nTMS patient had another seizure within the follow-up period, whereas four patients in the comparison group had further seizures. In the nTMS group, 1 of 4 patients with pre-op neurological deficits improved by one year; whereas the comparison group had increased neurological deficits in 3 of the 8 patients not having surgery. The median (range) change of tumor volume from baseline to 1 year was ?83 % (?67 % to ?100 %) in the nTMS group, but +12 % (+40 % to ?56 %) in the comparison group (p?<?0.001).

Conclusions

nTMS provides accurate motor mapping results also in infiltrative gliomas and enables more frequent and more extensive surgical resection of non-enhancing gliomas in or near the primary motor cortex. The substantial differences observed here in neurological and oncological outcomes suggest that further comparative research is warranted.     

Measurement of transcallosal inhibition in traumatic brain injury by transcranial magnetic stimulation

PRIMARY OBJECTIVE: To study whether transcallosal inhibition (TCI) can evaluate the severity of traumatic brain injury (TBI). RESEARCH DESIGN: Case-control study. METHODS AND PROCEDURES: Twenty patients with a chronic TBI and 20 control subjects were studied. The following transcranial magnetic stimulation parameters were checked; resting motor threshold, central motor latency times, onset latency of TCI, duration of TCI, transcallosal conduction times and amount of TCI. The severity of TBI was evaluated using the Glasgow Coma Scale (GCS). MAIN OUTCOME AND RESULTS: The amount of TCI was significantly lower in the patients than the control subjects (p < 0.001). The amount of TCI was highly correlated with the GCS (r = 0.787, p < 0.001). CONCLUSION: An assessment of TCI was found to be a more sensitive and useful method for an evaluation of the severity of TBI.     

Repetitive transcranial magnetic stimulation in veterans with debilitating tinnitus: a pilot study.

OBJECTIVE: Available evidence suggests tinnitus arises from excessive spontaneous activity in the left superior temporal gyrus, and repetitive transcranial magnetic stimulation (rTMS) may suppress this activity. Our hypothesis is that rTMS applied to this region would decrease tinnitus complaints in veterans. STUDY DESIGN: Prospective, nonrandomized trial. SUBJECTS AND METHODS: Eight patients with tinnitus received 5 consecutive days of rTMS (0.5 Hz, 20 minutes) to the left temporoparietal area. Tinnitus Handicap Inventory (THI) measures before sessions 1 and 3 and after session 5 were used to evaluate efficacy. RESULTS: Patient 1's THI decreased 40 to 34 to 26, patient 4 reported a subjective improvement, patient 8 withdrew, and the remaining patients reported no improvement. Adverse effects included temporary soreness, restlessness, and photophobia. CONCLUSION: The parameters for this rTMS study are different from those that reported success with its use. With these current parameters, rTMS did not improve tinnitus in veterans. There were no permanent adverse outcomes.     

Navigated transcranial magnetic stimulation for presurgical planning--correlation with functional MRI.

PURPOSE: This paper describes the potential of navigated transcranial magnetic stimulation to map the motor cortex in patients with mass lesions near the primary motor cortex by comparing the results of this technique to those of functional MRI. MATERIAL AND METHODS: Ten patients with mass lesions near the central sulcus were studied preoperatively using a figure-of-eight transcranial magnetic stimulator attached to a neuronavigation system to allow for direct visualization of the stimulated brain region. Subsequently, in all patients a blood oxygenation level dependent 2D multislice multishot T2*-weighted gradient echo EPI sequence on a 1.5 T Philips Gyroscan during motor activation was performed. Results of both methods were coregistered and compared. RESULTS: The distances between the peak parenchymal fMRI activation and the cortical area where TMS elicited the maximum MEPs ranged between 0 and 1.2 cm (mean 0.6 cm, SD 0.4 cm). CONCLUSION: We conclude that navigated TMS is a reliable alternative for localizing the motor-related areas in the human brain preoperatively and therefore may be a useful adjunct or, in selected patients, even a helpful alternative to functional MRI.     

Evaluation of thoracic myelopathy by transcranial magnetic stimulation

It is sometimes difficult to determine the appropriate surgical site in patients with thoracic myelopathy with diffuse or multisegmental lesions. To solve this problem, a magnetic stimulation study was carried out. Seven patients with myelopathy and 10 healthy control subjects were examined. Transcranial magnetic stimulation was applied and the motor evoked potentials (MEPs) of the intercostal muscles were recorded. The MEP latencies for the two groups were then compared. In patients with thoracic myelopathy, the MEP latencies caudal to the lesion were more extended than those of the control subjects. This method could identify the levels at which myelopathy originates in patients with a radiologically visible lesion. This method has the potential to be used for deciding the surgical site at the level responsible for myelopathy in cases with multiple or diffused compression.     

Combined temporal and prefrontal transcranial magnetic stimulation for tinnitus treatment: a pilot study.

OBJECTIVES: Low-frequency repetitive transcranial magnetic stimulation (rTMS) of the temporal cortex has been proposed as a new treatment strategy for patients with chronic tinnitus. However, functional abnormalities in tinnitus patients also involve brain structures used for attentional and emotional processing, such as the dorsolateral prefrontal cortex. Therefore, we have developed a new rTMS treatment strategy for tinnitus patients that consists of a combination of high-frequency prefrontal and low-frequency temporal rTMS. STUDY DESIGN: A total of 32 patients received either low-frequency temporal rTMS or a combination of high-frequency prefrontal and low-frequency temporal rTMS. Treatment effects were assessed with a standardized tinnitus questionnaire (TQ). RESULTS: Directly after therapy there was an improvement of the TQ-score for both groups, but no differences between groups. An evaluation after 3 months revealed a remarkable benefit from the use of combined prefrontal and temporal rTMS treatment. CONCLUSION: These results support recent data that suggest that auditory and nonauditory brain areas are involved in tinnitus pathophysiology.     

The planning and guiding of reading saccades: a repetitive transcranial magnetic stimulation study.

A previous positron emission tomography study that investigated the cortical areas involved in directing eye movements during text reading showed two areas of extra-occipital asymmetry: left > right posterior parietal cortex (PPC), and right > left frontal eye-field (FEF). We used the temporal resolution of repetitive TMS (rTMS) to isolate the contributions of the left and right PPC and FEF to the planning and execution of rightward reading saccades. We present eye-movement data collected during text reading, which involves the initiation and maintenance of a series of saccades (scanpath). rTMS over the left but not right PPC slowed reading speeds for the whole array of words, indicating that this area is involved throughout the scanpath. rTMS over the right but not the left FEF slowed the time to make the first saccade, but only when triggered before the stimuli appeared, demonstrating that the role of this region is in the preparation of the scanpath. Our results are compatible with the hypotheses that the left PPC maintains reading saccades along a line of text while the right FEF is involved in the preparation of the motor plan for the scanpath at the start of each new line of text.     

Imagery-induced cortical excitability changes in stroke: a transcranial magnetic stimulation study

Focal transcranial magnetic stimulation (TMS) was employed in a population of hemiparetic stroke patients in a post-acute stage to map out the abductor digiti minimi (ADM) muscle cortical representation of the affected (AH) and unaffected (UH) hemisphere at rest, during motor imagery and during voluntary contraction. Imagery induced an enhancement of the ADM map area and volume in both hemispheres in a way which partly corrected the abnormal asymmetry between AH and UH motor output seen in rest condition. The voluntary contraction was the task provoking maximal facilitation in the UH, whereas a similar degree of facilitation was obtained during voluntary contraction and motor imagery in the AH. We argued that motor imagery could induce a pronounced motor output enhancement in the hemisphere affected by stroke. Further, we demonstrated that imagery-induced excitability changes were specific for the muscle 'prime mover' for the imagined movement, while no differences were observed with respect to the stroke lesion locations. Present findings demonstrated that motor imagery significantly enhanced the cortical excitability of the hemisphere affected by stroke in a post-acute stage. Further studies are needed to correlate these cortical excitability changes with short-term plasticity therefore prompting motor imagery as a 'cortical reservoir' in post-stroke motor rehabilitation.