Naoto Kunii

A detailed analysis of functional magnetic resonance imaging in the frontal language area: a comparative study with extraoperative electrocortical stimulation.

BACKGROUND:Functional magnetic resonance imaging (fMRI) is a less invasive way of mapping brain functions. The reliability of fMRI for localizing language-related function is yet to be determined. OBJECTIVE:We performed a detailed analysis of language fMRI reliability by comparing the results of 3-T fMRI with maps determined by extraoperative electrocortical stimulation (ECS). METHODS:This study was performed on 8 epileptic patients who underwent subdural electrode placement. The tasks performed during fMRI included verb generation, abstract/concrete categorization, and picture naming. We focused on the frontal lobe, which was effectively activated by these tasks. In extraoperative ECS, 4 tasks were combined to determine the eloquent areas: spontaneous speech, picture naming, reading, and comprehension. We calculated the sensitivity and specificity with different Z score thresholds for each task and appropriate matching criteria. For further analysis, we divided the frontal lobe into 5 areas and investigated intergyrus variations in sensitivity and specificity. RESULTS:The abstract/concrete categorization task was the most sensitive and specific task in fMRI, whereas the picture naming task detected eloquent areas most efficiently in ECS. The combination of the abstract/concrete categorization task and a 3-mm matching criterion gave the best tradeoff (sensitivity, 83%; specificity, 61%) when the Z score was 2.24. As for intergyrus variation, the posterior inferior frontal gyrus showed the best tradeoff (sensitivity, 91%; specificity, 59%), whereas the anterior middle frontal gyrus had low specificity. CONCLUSION:Despite different tasks for fMRI and extraoperative ECS, the relatively low specificity might be caused by a fundamental discrepancy between the 2 techniques. Reliability of language fMRI activation might differ, depending on the brain region.

Outcomes of Diffusion Tensor Tractography–Integrated Stereotactic Radiosurgery

PURPOSE To analyze the effect of use of tractography of the critical brain white matter fibers created from diffusion tensor magnetic resonance imaging on reduction of morbidity associated with radiosurgery. METHODS AND MATERIALS Tractography of the pyramidal tract has been integrated since February 2004 if lesions are adjacent to it, the optic radiation since May 2006, and the arcuate fasciculus since October 2007. By visually confirming the precise location of these fibers, the dose to these fiber tracts was optimized. One hundred forty-four consecutive patients with cerebral arteriovenous malformations who underwent radiosurgery with this technique between February 2004 and December 2009 were analyzed. RESULTS Tractography was prospectively integrated in 71 of 155 treatments for 144 patients. The pyramidal tract was visualized in 45, the optic radiation in 22, and the arcuate fasciculus in 13 (two tracts in 9). During the follow-up period of 3 to 72 months (median, 23 months) after the procedure, 1 patient showed permanent worsening of pre-existing dysesthesia, and another patient exhibited mild transient hemiparesis 12 months later but fully recovered after oral administration of corticosteroid agents. Two patients had transient speech disturbance before starting integration of the arcuate fasciculus tractography, but no patient thereafter. CONCLUSION Integrating tractography helped prevent morbidity of radiosurgery in patients with brain arteriovenous malformations.

Characteristic profiles of high gamma activity and blood oxygenation level-dependent responses in various language areas.

High gamma activity (HGA) has been shown to be positively correlated with blood oxygenation level-dependent (BOLD) responses in the primary cortices with simple tasks. It is, however, an open question whether the correlation is simply applied to the association areas related to higher cognitive functions. The aim of this study is to investigate quantitative correlation between HGA and BOLD and their spatial and temporal profiles during semantic processing. Thirteen patients with intractable epilepsy underwent fMRI and electrocorticography (ECoG) with a word interpretation task to evoke language-related responses. Percent signal change of BOLD was calculated at each site of ECoG electrode, which has power amplification of high gamma band (60-120 Hz) activity. We transformed locations of individual electrodes and brains to a universal coordination using SPM8 and made the quantitative comparisons on a template brain. HGAs were increased in several language-related areas such as the inferior frontal and middle temporal gyri and were positively correlated with BOLD responses. The most striking finding was different temporal dynamics of HGAs in the different brain regions. Whereas the frontal lobe showed longer-lasting HGA, the HGA-intensity on the temporal lobe quickly declined. The different temporal dynamics of HGA might explain why routine language-fMRI hardly detected BOLD in the temporal lobe. This study clarified different neural oscillation and BOLD response in various brain regions during semantic processing and will facilitate practical utilization of fMRI for evaluating higher-order cognitive functions not only in basic neuroscience, but also in clinical practice.

The dynamics of language-related high-gamma activity assessed on a spatially-normalized brain

OBJECTIVE We developed a novel technique of spatial normalization of subdural electrode positions across subjects and assessed the spatial-temporal dynamics of high-gamma activity (HGA) in the dominant hemisphere elicited by three distinct language tasks. METHODS The normalization process was applied to 1512 subdural electrodes implanted in 21 patients with intractable epilepsy. We projected each task-related HGA profile onto a normalized brain. RESULTS The word interpretation task initially elicited HGA augmentation in the bilateral fusiform gyri at 100 ms after stimulus onsets, subsequently in the left posterior middle temporal gyrus, in the left ventral premotor cortex at 200 ms and in the left middle and left inferior frontal gyri at 300 ms and after. The picture naming task elicited HGA augmentation in few sites in the left frontal lobe. The verb generation task elicited HGA in the left superior temporal gyrus at 100-600 ms. Common HGA augmentation elicited by all three tasks was noted in the left posterior-middle temporal and left ventral premotor cortices. CONCLUSIONS The spatial-temporal dynamics of language-related HGA were demonstrated on a spatially-normalized brain template. SIGNIFICANCE This study externally validated the spatial and temporal dynamics of language processing suggested by previous neuroimaging and electrophysiological studies.

Angiographic Classification of Tumor Attachment of Meningiomas at the Cerebellopontine Angle

OBJECTIVE To present an angiographic classification of attachment of meningiomas at the cerebellopontine angle (CPA) based on tumor feeding and to validate the utility of this classification in predicting meningioma attachments at the CPA. METHODS The authors retrospectively analyzed 34 consecutive patients with meningioma at the CPA. Based on operative findings, tumors were classified into four types: the petroclival type, in which the trigeminal nerve is displaced laterally; the tentorial type, in which the center of tumor attachment is located at the medial tentorium; the anterior petrous type, in which the center of tumor attachment is located anterior to the meatus; and the posterior petrous type, in which the center of tumor attachment is located posterior to the meatus. Magnetic resonance imaging (MRI) was sufficient to confirm attachment of the posterior petrous type. Another 26 cases were analyzed angiographically and classified into three types: abnormal ipsilateral tentorial artery type (type A); bilateral internal carotid artery (ICA) type (type B); and nontentorial, non-ICA type (type N). This angiographic classification was validated by comparison with the attachment classification. RESULTS Angiographic types A, B, and N corresponded to tentorial, petroclival, and anterior petrous types of attachment. Observed agreement was very high, particularly for tumors greater than 30 mm in diameter (κ statistic 0.83; 95% confidence interval [CI] 0.62-1.0). Angiographic type in this paired attachment typing offered high sensitivity and specificity greater than 0.80 in tumors larger than 30 mm. CONCLUSIONS This angiographic classification seems to be useful in predicting meningioma attachments at the CPA. The existence of an abnormally developed tentorial artery seems highly indicative of tumor attachment to the tentorium.

Osteomalacia caused by skull base tumors: report of 2 cases.

BACKGROUND AND IMPORTANCE:Tumor-induced osteomalacia (TIO) is an uncommon paraneoplastic syndrome rarely encountered in neurosurgical practice. We report on 2 cases of TIO caused by skull base tumors. Although the diagnosis of TIO is difficult to make and often is delayed because of the insidious nature of the symptoms, mostly systemic pain and weakness, it is curable once it is diagnosed and properly treated. CLINICAL PRESENTATION:Both patients presented with severe pain developing in the lower extremities and moving out to the entire body, as well as difficulty moving. They were diagnosed with TIO several years after onset. A high level of serum FGF23 was confirmed, and whole-body imaging studies demonstrated tumors in the middle and anterior cranial base, respectively. The patient with the anterior cranial base tumor had a history of hemorrhage into the frontal lobe and partial resection. En bloc resection of tumor with surrounding skull bone was performed. The histological diagnosis for both cases was phosphaturic mesenchymal tumor, mixed connective tissue variant. CONCLUSION:The level of FGF23 normalized immediately after surgery. Both patients experienced a dramatic relief of pain and recovery of muscle power. Although reports of osteomalacia caused by tumors in the neurosurgical field are extremely rare in the literature, its true incidence is unknown. We emphasize the importance of recognition of this syndrome and recommend total resection of tumors when possible.

The significance of parahippocampal high gamma activity for memory preservation in surgical treatment of atypical temporal lobe epilepsy

Resective surgery for mesial temporal lobe epilepsy (MTLE) with a correspondent lesion has been established as an effective and safe procedure. Surgery for temporal lobe epilepsies with bilateral hippocampal sclerosis or without correspondent lesions, however, carries a higher risk of devastating memory decline, underscoring the importance of establishing the memory‐dominant side preoperatively and adopting the most appropriate procedure. In this study, we focused on high gamma activities (HGAs) in the parahippocampal gyri and investigated the relationship between memory‐related HGAs and memory outcomes after hippocampal transection (HT), a hippocampal counterpart to neocortical multiple subpial transection. The transient nature of memory worsening after HT provided us with a rare opportunity to compare HGAs and clinical outcomes without risking permanent memory disorders.

Machine Learning of DTI Structural Brain Connectomes for Lateralization of Temporal Lobe Epilepsy

BACKGROUND AND PURPOSE We analyzed the ability of a machine learning approach that uses diffusion tensor imaging (DTI) structural connectomes to determine lateralization of epileptogenicity in temporal lobe epilepsy (TLE). MATERIALS AND METHODS We analyzed diffusion tensor and 3-dimensional (3D) T1-weighted images of 44 patients with TLE (right, 15, left, 29; mean age, 33.0 ± 11.6 years) and 14 age-matched controls. We constructed a whole brain structural connectome for each subject, calculated graph theoretical network measures, and used a support vector machine (SVM) for classification among 3 groups (right TLE versus controls, left TLE versus controls, and right TLE versus left TLE) following a feature reduction process with sparse linear regression. RESULTS In left TLE, we found a significant decrease in local efficiency and the clustering coefficient in several brain regions, including the left posterior cingulate gyrus, left cuneus, and both hippocampi. In right TLE, the right hippocampus showed reduced nodal degree, clustering coefficient, and local efficiency. With use of the leave-one-out cross-validation strategy, the SVM classifier achieved accuracy of 75.9 to 89.7% for right TLE versus controls, 74.4 to 86.0% for left TLE versus controls, and 72.7 to 86.4% for left TLE versus right TLE. CONCLUSION Machine learning of graph theoretical measures from the DTI structural connectome may give support to lateralization of the TLE focus. The present good discrimination between left and right TLE suggests that, with further refinement, the classifier should improve presurgical diagnostic confidence.

Dissociated Roles of the Inferior Frontal Gyrus and Superior Temporal Sulcus in Audiovisual Processing: Top-Down and Bottom-Up Mismatch Detection

Visual inputs can distort auditory perception, and accurate auditory processing requires the ability to detect and ignore visual input that is simultaneous and incongruent with auditory information. However, the neural basis of this auditory selection from audiovisual information is unknown, whereas integration process of audiovisual inputs is intensively researched. Here, we tested the hypothesis that the inferior frontal gyrus (IFG) and superior temporal sulcus (STS) are involved in top-down and bottom-up processing, respectively, of target auditory information from audiovisual inputs. We recorded high gamma activity (HGA), which is associated with neuronal firing in local brain regions, using electrocorticography while patients with epilepsy judged the syllable spoken by a voice while looking at a voice-congruent or -incongruent lip movement from the speaker. The STS exhibited stronger HGA if the patient was presented with information of large audiovisual incongruence than of small incongruence, especially if the auditory information was correctly identified. On the other hand, the IFG exhibited stronger HGA in trials with small audiovisual incongruence when patients correctly perceived the auditory information than when patients incorrectly perceived the auditory information due to the mismatched visual information. These results indicate that the IFG and STS have dissociated roles in selective auditory processing, and suggest that the neural basis of selective auditory processing changes dynamically in accordance with the degree of incongruity between auditory and visual information.

Simultaneous recording of single-neuron activities and broad-area intracranial electroencephalography: electrode design and implantation procedure.

BACKGROUND: There has been growing interest in clinical single-neuron recording to better understand epileptogenicity and brain function. It is crucial to compare this new information, single-neuronal activity, with that obtained from conventional intracranial electroencephalography during simultaneous recording. However, it is difficult to implant microwires and subdural electrodes during a single surgical operation because the stereotactic frame hampers flexible craniotomy. OBJECTIVE: To describe newly designed electrodes and surgical techniques for implanting them with subdural electrodes that enable simultaneous recording from hippocampal neurons and broad areas of the cortical surface. METHODS: We designed a depth electrode that does not protrude into the dura and pulsates naturally with the brain. The length and tract of the depth electrode were determined preoperatively between the lateral subiculum and the lateral surface of the temporal lobe. A frameless navigation system was used to insert the depth electrode. Surface grids and ventral strips were placed before and after the insertion of the depth electrodes, respectively. Finally, a microwire bundle was inserted into the lumen of the depth electrode. We evaluated the precision of implantation, the recording stability, and the recording rate with microwire electrodes. RESULTS: Depth-microwire electrodes were placed with a precision of 3.6 mm. The mean successful recording rate of single- or multiple-unit activity was 14.8%, which was maintained throughout the entire recording period. CONCLUSION: We achieved simultaneous implantation of microwires, depth electrodes, and broad-area subdural electrodes. Our method enabled simultaneous and stable recording of hippocampal single-neuron activities and multichannel intracranial electroencephalography. ABBREVIATIONS: iEEG, intracranial electroencephalography LFP, local field potential