Motor Mapping with Functional Magnetic Resonance Imaging: Comparison with Electrical Cortical Stimulation

The aim of the present study was to evaluate motor area mapping using functional magnetic resonance imaging (fMRI) compared with electrical cortical stimulation (ECS). Motor mapping with fMRI and ECS were retrospectively compared in seven patients with refractory epilepsy in which the primary motor (M1) areas were identified by fMRI and ECS mapping between 2012 and 2019. A right finger tapping task was used for fMRI motor mapping. Blood oxygen level-dependent activation was detected in the left precentral gyrus (PreCG)/postcentral gyrus (PostCG) along the “hand knob” of the central sulcus in all seven patients. Bilateral supplementary motor areas (SMAs) were also activated (n = 6), and the cerebellar hemisphere showed activation on the right side (n = 3) and bilateral side (n = 4). Furthermore, the premotor area (PM) and posterior parietal cortex (PPC) were also activated on the left side (n = 1) and bilateral sides (n = 2). The M1 and sensory area (S1) detected by ECS included fMRI-activated PreCG/PostCG areas with broader extent. This study showed that fMRI motor mapping was locationally well correlated to the activation of M1/S1 by ECS, but the spatial extent was not concordant. In addition, the involvement of SMA, PM/PPC, and the cerebellum in simple voluntary movement was also suggested. Combination analysis of fMRI and ECS motor mapping contributes to precise localization of M1/S1.     

Evaluation of Language Function under Awake Craniotomy

Awake craniotomy is the only established way to assess patients’ language functions intraoperatively and to contribute to their preservation, if necessary. Recent guidelines have enabled the approach to be used widely, effectively, and safely. Non-invasive brain functional imaging techniques, including functional magnetic resonance imaging and diffusion tensor imaging, have been used preoperatively to identify brain functional regions corresponding to language, and their accuracy has increased year by year. In addition, the use of neuronavigation that incorporates this preoperative information has made it possible to identify the positional relationships between the lesion and functional regions involved in language, conduct functional brain mapping in the awake state with electrical stimulation, and intraoperatively assess nerve function in real time when resecting the lesion. This article outlines the history of awake craniotomy, the current state of pre- and intraoperative evaluation of language function, and the clinical usefulness of such functional evaluation. When evaluating patients’ language functions during awake craniotomy, given the various intraoperative stresses involved, it is necessary to carefully select the tasks to be undertaken, quickly perform all examinations, and promptly evaluate the results. As language functions involve both input and output, they are strongly affected by patients’ preoperative cognitive function, degree of intraoperative wakefulness and fatigue, the ability to produce verbal articulations and utterances, as well as perform synergic movement. Therefore, it is essential to appropriately assess the reproducibility of language function evaluation using awake craniotomy techniques.     

Integrated image- and function-guided surgery in eloquent cortex: a technique report

The ability to effectively identify eloquent cortex in close proximity to brain tumours is a critical component of surgical planning prior to resection. The use of electrocortical stimulation testing (ECS) during awake neurosurgical procedures remains the gold standard for mapping functional areas, yet the preoperative use of non-invasive brain imaging techniques such as fMRI are gaining popularity as supplemental surgical planning tools. In addition, the intraoperative three-dimensional display of fMRI findings co-registered to structural imaging data maximizes the utility of the preoperative mapping for the surgeon. Advances in these techniques have the potential to limit the size and duration of craniotomies as well as the strain placed on the patient, but more research accurately demonstrating their efficacy is required. In this paper, we demonstrate the integration of preoperative fMRI within a neuronavigation system to aid in surgical planning, as well as the integration of these fMRI data with intraoperative ECS mapping results into a three-dimensional dataset for the purpose of cross-validation.     

Intraoperative Motor Symptoms during Brain Tumor Resection in the Supplementary Motor Area (SMA) without Positive Mapping during Awake Surgery

Awake surgery could be a useful modality for lesions locating in close proximity to the eloquent areas including primary motor cortex and pyramidal tract. In case with supplementary motor area (SMA) lesion, we often encounter with intraoperative motor symptoms during awake surgery even in area without positive mapping. Although the usual recovery of the SMA syndrome has been well documented, rare cases with permanent deficits could be encountered in the clinical setting. It has been difficult to evaluate during surgery whether the intraoperative motor symptoms lead to postoperative permanent deficits. The purpose of this study was to demonstrate the intraoperative motor symptoms could be reversible, further to provide useful information for making decision to continue surgical procedure of tumor resection. Eight consecutive patients (from July 2012 to June 2014, six men and two women, aged 33–63 years) with neoplastic lesions around the SMA underwent an awake surgery. Using a retrospective analysis of intraoperative video records, intraoperative motor symptoms during tumor resection were investigated. In continuous functional monitoring during resection of SMA tumor under awake conditions, the following motor symptoms were observed during resection of the region without positive mapping: delayed motor weakness, delay of movement initiation, slowness of movement, difficulty in dual task response, and coordination disturbance. In seven patients hemiparesis observed immediately after surgery recovered to preoperative level within 6 weeks. During awake surgery for SMA tumors, the above-mentioned motor symptoms could occur in area without positive mapping and might be predictors for reversible SMA syndrome.     

Novel Techniques of Real-time Blood Flow and Functional Mapping: Technical Note

There are two main approaches to intraoperative monitoring in neurosurgery. One approach is related to fluorescent phenomena and the other is related to oscillatory neuronal activity. We developed novel techniques to visualize blood flow (BF) conditions in real time, based on indocyanine green videography (ICG-VG) and the electrophysiological phenomenon of high gamma activity (HGA). We investigated the use of ICG-VG in four patients with moyamoya disease and two with arteriovenous malformation (AVM), and we investigated the use of real-time HGA mapping in four patients with brain tumors who underwent lesion resection with awake craniotomy. Real-time data processing of ICG-VG was based on perfusion imaging, which generated parameters including arrival time (AT), mean transit time (MTT), and BF of brain surface vessels. During awake craniotomy, we analyzed the frequency components of brain oscillation and performed real-time HGA mapping to identify functional areas. Processed results were projected on a wireless monitor linked to the operating microscope. After revascularization for moyamoya disease, AT and BF were significantly shortened and increased, respectively, suggesting hyperperfusion. Real-time fusion images on the wireless monitor provided anatomical, BF, and functional information simultaneously, and allowed the resection of AVMs under the microscope. Real-time HGA mapping during awake craniotomy rapidly indicated the eloquent areas of motor and language function and significantly shortened the operation time. These novel techniques, which we introduced might improve the reliability of intraoperative monitoring and enable the development of rational and objective surgical strategies.     

Multimodal protocol for awake craniotomy in language cortex tumour surgery

Summary Background. Intra-operative neurophysiological language mapping has become an established procedure in patients operated on for tumours in the area of the language cortex. Awake cranial surgery has specific risks and patients are exposed to an increased physical and mental stress. The aim of the study was to establish an algorithm that enables tailoring the neurosurgical and anaesthetic techniques to the individual patient. Method. A total of 25 patients underwent awake craniotomy for intra-operative language mapping between 1999 and 2004. Following craniotomy under analgesia and sedation without rigid pin fixation of the head, cortical language mapping was performed in the fully co-operative patient. The results of functional magnetic resonance imaging and of cortical language mapping were incorporated into the 3D dataset for neuronavigation. Depending on the functional data and the individual operative risk tumour resection then proceeded either under conscious sedation with the option of subcortical language monitoring or under general anaesthesia. Findings. After cortical language mapping patients are assigned to one of four groups: BACC (Berlin awake craniotomy criteria) I–IV. BACC I (9 patients): adequate functional data + operative risk not increased ⇒ tumour resection in the awake patient; BACC II (4 patients): limited functional data + operative risk not increased ⇒ tumour resection in the awake patient with the option of language monitoring as needed; BACC III (9 patients): adequate functional data + increased operative risk ⇒ tumour resection under general anaesthesia using functional navigation; BACC IV (3 patients): limited functional data + increased operative risk ⇒ tumour resection in the awake patient with the option of language monitoring as needed. We observed less adverse events in group BACC III. No permanent deterioration of language function occurred in this series. Conclusions. The multimodal protocol for awake craniotomy provides for tumour resection under general anaesthesia in selected patients using functional neuronavigation. Our experience with the algorithm suggests that it is a useful tool for preserving function in patients undergoing surgery of the language cortex while reducing the operative risk on an individual basis.     

Discordance between functional magnetic resonance imaging during silent speech tasks and intraoperative speech arrest

OBJECT: The goal of this study was to investigate discordance between the location of speech arrest during awake cortical mapping, a common intraoperative indicator of hemispheric dominance, and silent speech functional magnetic resonance (fMR) imaging maps of frontal language function. METHODS: Twenty-one cases were reviewed retrospectively. Images of silent speech fMR imaging activation were coregistered to anatomical MR images obtained for neuronavigation. These were compared with the intraoperative cortical photographs and the behavioral results of electrocorticography during awake craniotomy. An fMR imaging control study of three healthy volunteers was then conducted to characterize the differences between silent and vocalized speech fMR imaging protocols used for neurosurgical planning. CONCLUSIONS: Results of fMR imaging showed consistent and predominant activation of the inferior frontal gyrus (IFG) during silent speech tasks. During intraoperative mapping, however, 16 patients arrested in the precentral gyrus (PRG), well posterior to the fMR imaging activity. Of those 16, 14 arrested only in the PRG and not in the IFG as silent speech fMR imaging predicted. The control fMR imaging study showed that vocalized speech fMR imaging shifts the location of the fMR imaging prediction to include the motor strip and may be more appropriate for neurosurgical planning.     

3.0T术中磁共振成像引导下唤醒麻醉联合术中语言皮质定位技术在语言区脑胶质瘤手术中的应用

目的 评价3.0 T术中磁共振成像(iMRI)下采用唤醒麻醉联合术中语言皮质定位技术辅助语言区脑胶质瘤切除的临床有效性.方法 2010年12月至2011年4月以集成3.0 TiMRI数字一体化神经外科手术中心为平台,采用唤醒麻醉、改良手术铺巾技术、联合直接电刺激语言皮质定位和iMRI实时影像神经导航,对11例右利手患者实施左侧语言区脑胶质瘤切除.术中采用简易语言任务模式,包括语言流利度、图片命名和文字测读,评估患者语言功能状况.围手术期采用汉语失语检查法,评估新技术的临床有效性.结果 通过iMRI实时影像导航,6/11的患者可以定量提升胶质瘤切除范围,其中影像学全切除率提高3/11,最终肿瘤全切除7例,次全切除4例.语言皮质定位阳性率为8/11.患者术后1周内出现一过性失语率为4/11,随访至术后1个月,所有患者语言功能均恢复到术前水平或以上;围手术期患者无肢体运动功能障碍.结论 应用3.0 T超高场强iMRI实时影像导航可在术前设计脑胶质瘤个体化手术方案,术中精确定位病灶,等体积定量切除肿瘤,提高肿瘤切除率;在唤醒麻醉下实施术中皮质电刺激定位语言区,能最大程度保护患者语言皮质,避免出现不可逆的语言功能损伤,提高术后社会生活质量.

Abstract：

Objectives To evaluate preliminary clinical experience for combining awake craniotomy and intraoperative language brain mapping within the integrated 3.0 T intraoperative maguetic resonance imaging (iMRI) suite.Methods From December 2010 to April 2011,11 right hand-dominant patients with left glioma were involved in, or adjacent to, eloquent cortex was carried out awake craniotomies with cortical stimulation within an integrated 3.0 T iMRI suite.Aphasia battery of Chinese was used to test the language function before the operation.During the procedure, after the occipital, temporal, and supraorbital nerves were blocked by the anesthesiologists, the head was fixed with a custom high-field MRI-compatible head holder.The skull and dura was opened as usual and language brain mapping was then performed.Language testing followed a set protocol:counting numbers from 1 to 50, naming objects, reading single words.Resection of the tumor was guided by neuronavigation system and continued until eloquent areas were encountered or the margin of assessment was reached.An interdissection MRI was aquired to evaluate the glioma removal in a movable MRI scanner after minimal draping. Meanwhile, adverse effects caused by electrical stimulation and iMRI were recorded.The follow-up speech tests were assessed on 7th day and 1 month at least after the operation.Results The combined use of 3.0 T iMRI and awake craniotomy was performed safely in all patients.No adverse effects were reported.The duration of surgery was prolonged by 2 to 4 h.The patients' perception of iMRI during surgery was favorable.First-look MRI studies led to further resection attempts in 6/11 cases as well as a 3/11 increase in the number of gross-total resections.One week after surgery, baseline language function worsened in 4 cases. However, no patients had a persistent language deficit one month after surgery. Conclusions Awake craniotomy and direct cortical electrical stimulation can be performed safely and effectively within a 3.0 T iMRI suite.The combination of high-field iMRI and awake craniotomy may facilitate safe removal of eloquent glioma.     

Awake craniotomy using initial sleep with laryngeal mask airway in depressed agitated patient--a case report

Depressed patients with brain tumors are often not referred to awake craniotomy because of concern of uncooperation which may increase the risk of perioperative complications. This report describes an interesting case of Awake Craniotomy for frontal lobe glioma in 41 year old woman undergoing language and motor mapping intra-operatively. As she was fearful and apprehensive and was on antidepressant therapy to control depression the author adapted general anesthesia with laryngeal mask airway during initial stage of skull pinning and craniotomy procedures. Then patient reverted to awake state to continue the intended neurosurgical procedure. Patient tolerated the situation satisfactory and was cooperative till the finish without any event.     

Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation

OBJECTIVE: The aim of this study was to analyze the usefulness of preoperative language functional magnetic resonance imaging (fMRI), by correlating fMRI data with intraoperative cortical stimulation results for patients with brain tumors. METHODS: Naming and verb generation tasks were used, separately or in combination, for 14 right-handed patients with tumors in the left hemisphere. fMRI data obtained were analyzed with SPM software, with two standard analysis thresholds (P < 0.005 and then P < 0.05). The fMRI data were then registered in a frameless stereotactic neuronavigational device and correlated with direct brain mapping results. We used a statistical model with the fMRI information as a predictor, spatially correlating each intraoperatively mapped cortical site with fMRI data integrated in the neuronavigational system (site-by-site correlation). Eight patients were also studied with language fMRI postoperatively, with the same acquisition protocol. RESULTS: We observed high variability in signal extents and locations among patients with both tasks. The activated areas were located mainly in the left hemisphere in the middle and inferior frontal gyri (F2 and F3), the superior and middle temporal gyri (T1 and T2), and the supramarginal and angular gyri. A total of 426 cortical sites were tested for each task among the 14 patients. In frontal and temporoparietal areas, poor sensitivity of the fMRI technique was observed for the naming and verb generation tasks (22 and 36%, respectively) with P < 0.005 as the analysis threshold. Although not perfect, the specificity of the fMRI technique was good in all conditions (97% for the naming task and 98% for the verb generation task). Better correlation (sensitivity, 59%; specificity, 97%) was achieved by combining the two fMRI tasks. Variation of the analysis threshold to P < 0.05 increased the sensitivity to 66% while decreasing the specificity to 91%. Postoperative fMRI data (for the cortical brain areas studied intraoperatively) were in accordance with brain mapping results for six of eight patients. Complete agreement between pre- and postoperative fMRI studies and direct brain mapping results was observed for only three of eight patients. CONCLUSION: With the paradigms and analysis thresholds used in this study, language fMRI data obtained with naming or verb generation tasks, before and after surgery, were imperfectly correlated with intraoperative brain mapping results. A better correlation could be obtained by combining the fMRI tasks. The overall results of this study demonstrated that language fMRI could not be used to make critical surgical decisions in the absence of direct brain mapping. Other acquisition protocols are required for evaluation of the potential role of language fMRI in the accurate detection of essential cortical language areas.     

Present state of anesthetic management for awake craniotomy in Japan

To avoid the neurological deficits after neurosurgical procedures, awake craniotomy applying intraoperative awake functional brain mapping has been employed. Anesthesia for awake craniotomy requires particular attention to airway management, control of seizures and measures for decreasing the anxiety of the patients. We investigated the current status of anesthetic management for awake craniotomy in Japan to establish a standard procedure for safe anesthesia. A questionnaire was sent to 80 universities with departments of anesthesia in Japan and 34 (43%) responded. In 19 institutes, awake craniotomies are being practiced. The first experience of awake craniotomy was in 1996 in Japan and since then most of the institutes have experienced only three or fewer cases. Airway management, control of nausea and vomiting, stable awakening during functional mapping and control of seizures were pointed out as problems during awake craniotomy. Based on the present results, our experience and the information from previous investigations, standard anesthetic management for awake craniotomy in our country will be documented.     

Preoperative fMRI, tractography and continuous task during awake surgery for maintenance of motor function following surgical resection of metastatic tumor spread to the primary motor area.

The goal of the present study was to determine the efficacy of preoperative fMRI, tractography, and intraoperative continuous task during awake surgery in preserving postoperative motor function in patients undergoing resection of metastatic brain tumors in or near the primary motor area. Three patients with metastatic brain tumors in the primary motor area elected to undergo surgical treatment. Preoperative fMRI and tractography were performed, and various primary motor areas (e. g., hand, arm, face and leg) were identified and confirmed by cortical mapping or by the outcome of awake surgery. Cortical mapping and continuous appropriate task were performed during awake surgery. Preoperative fMRI and tractography correctly identified the primary motor area. In contrast, cortical mapping identified the gyrus of the primary motor area but was unable to identify specific primary motor areas, such as those for the hand or arm, which were compressed by the tumor. Tumor resection was terminated when any deterioration in continuous task performance was observed during awake surgery. Paresis was transient and resolved within one week in all cases. The combination of preoperative fMRI, tractography and continuous task during awake surgery helped to maintain motor function following surgical management of metastatic brain tumors of the primary motor cortex.     

Clinical features and significance of negative motor response in intraoperative language mapping during awake craniotomy

The negative motor area and anterior and posterior language areas were localized by intraoperative electrical cortical stimulation under the awake condition to evaluate the clinical significance of these areas. Thirty-seven awake craniotomies with language mapping were performed in 36 patients with brain tumors. The negative motor area was determined in 17 cases, and the anterior and posterior language areas were found in 12 and 6 cases, respectively. The negative motor area was located in the precentral gyrus inferior to the orofacial motor area in 16 cases, and in the inferior frontal gyrus anterior to the orofacial motor area in one case. Both the negative motor area and the anterior language area were determined in 8 cases. Anterior language areas in these 8 cases were located anterior and/or inferior to the negative motor areas. The negative motor area is an easily determined, important landmark for intraoperative language mapping.     

The use of continuous positive airway pressure during an awake craniotomy in a patient with obstructive sleep apnea

We describe the anesthetic management of a morbidly obese patient with obstructive sleep apnea who underwent awake craniotomy. The patient's personal continuous positive airway pressure (CPAP) machine was used to support ventilation intraoperatively. Dexmedetomidine was used as the primary sedative. During cortical mapping, the CPAP was discontinued. The patient was comfortable and able to cooperate with language testing.     

Distinct neural substrates for semantic knowledge and naming in the temporoparietal network

Patients with anterior temporal lobe (ATL) lesions show semantic and lexical retrieval deficits, and the differential role of this area in the 2 processes is debated. Functional neuroimaging in healthy individuals has not clarified the matter because semantic and lexical processes usually occur simultaneously and automatically. Furthermore, the ATL is a region challenging for functional magnetic resonance imaging (fMRI) due to susceptibility artifacts, especially at high fields. In this study, we established an optimized ATL-sensitive fMRI acquisition protocol at 4 T and applied an event-related paradigm to study the identification (i.e., association of semantic biographical information) of celebrities, with and without the ability to retrieve their proper names. While semantic processing reliably activated the ATL, only more posterior areas in the left temporal and temporal-parietal junction were significantly modulated by covert lexical retrieval. These results suggest that within a temporoparietal network, the ATL is relatively more important for semantic processing, and posterior language regions are relatively more important for lexical retrieval.     

Use of the laryngeal mask airway during awake craniotomy for tumor resection

There is an increasing trend toward performing craniotomy for primary brain tumor excision with local anesthesia. We report the use of the laryngeal mask airway as a part of an anesthetic technique designed for patients requiring awake cortical mapping during brain tumor excision.     

Resting-state functional connectivity of the medial superior frontal cortex

The medial superior frontal cortex (SFC), including the supplementary motor area (SMA) and presupplementary motor area (preSMA), is implicated in movement and cognitive control, among other functions central to decision making. Previous studies delineated the anatomical boundaries and functional connectivity of the SMA. However, it is unclear whether the preSMA, which responds to a variety of behavioral tasks, comprises functionally distinct areas. With 24 seed regions systematically demarcated throughout the anterior and posterior medial SFC, we examined here the functional divisions of the medial SFC on the basis of the "correlograms" of resting-state functional magnetic resonance imaging data of 225 adult individuals. In addition to replicating segregation of the SMA and posterior preSMA, the current results elucidated functional connectivities of anterior preSMA-the most anterior part of the medial SFC. In contrast to the caudal medial SFC, the anterior preSMA is connected with most of the prefrontal but not with somatomotor areas. Overall, the SMA is strongly connected to the thalamus and epithalamus, the posterior preSMA to putamen, pallidum, and subthalamic nucleus, and anterior preSMA to the caudate, with the caudate showing significant hemispheric asymmetry. These findings may provide a useful platform for future studies to investigate frontal cortical functions.     

Color discrimination involves ventral and dorsal stream visual areas

We used positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) in human subjects to investigate whether the ventral and dorsal visual stream cooperate when active judgements about color have to be made. Color was used as the attribute, because it is processed primarily in the ventral stream. The centrally positioned stimuli were equiluminant shades of brown. The successive color discrimination task was contrasted to a dimming detection task, in which retinal input was identical but with double the number of motor responses. The stimulus presentation rate was parametrically varied and a constant performance level was obtained for all conditions. The visual activation sites were identified by retinotopic mapping and cortical flattening. In addition, one psychophysical and two fMRI experiments were performed to control for differences in visuospatial attention and motor output. Successive color discrimination involved early visual areas, including V1 and VP and the ventral color-responsive region, as well as anterior and middle dorsal intraparietal sulcus, dorsal premotor cortex and pre-SMA. Cortical regions involved in dimming detection and motor output included area V3A, hMT/V5+, lateral occipital sulcus, posterior dorsal intraparietal sulcus, primary motor cortex and SMA. These experiments demonstrated that even with color as the attribute, successive discrimination, in which a decision process has to link visual signals to motor responses, involves both ventral and dorsal visual stream areas.     

Patient response to awake craniotomy – a summary overview

Background

Awake craniotomy is a valuable procedure since it allows brain mapping and live monitoring of eloquent brain functions. The advantage of minimizing resource utilization is also emphasized by some physicians in North America. Data on how well an awake craniotomy is tolerated by patients and how much stress it creates is available from different studies, but this topic has not consequently been summarized in a review of the available literature. Therefore, it is the purpose of this review to shed more light on the still controversially discussed aspect of an awake craniotomy.

Methods

We reviewed the available English literature published until December 2013 searching for studies that investigated patients’ responses to awake craniotomies.

Results

Twelve studies, published between 1998 and 2013, including 396 patients with awake surgery were identified. Eleven of these 12 studies set the focus on the perioperative time, one study focused on the later postoperative time. The vast majority of patients felt well prepared and overall satisfaction with the procedure was high. In the majority of studies up to 30 % of the patients recalled considerable pain and 10–14 % experienced strong anxiety during the procedure. The majority of patients reported that they would undergo an awake craniotomy again. A post traumatic stress disorder was present neither shortly nor years after surgery. However, a normal human response to such an exceptional situation can for instance be the delayed appearance of unintentional distressing recollections of the event despite the patients’ satisfaction concerning the procedure.

Conclusions

For selected patients, an awake craniotomy presents the best possible way to reduce the risk of surgery related neurological deficits. However, benefits and burdens of this type of procedure should be carefully considered when planning an awake craniotomy and the decision should serve the interests of the patient.