Mapping cognitive and emotional networks in neurosurgical patients using resting-state functional magnetic resonance imaging.

Neurosurgery has been at the forefront of a paradigm shift from a localizationist perspective to a network-based approach to brain mapping. Over the last 2 decades, we have seen dramatic improvements in the way we can image the human brain and noninvasively estimate the location of critical functional networks. In certain patients with brain tumors and epilepsy, intraoperative electrical stimulation has revealed direct links between these networks and their function. The focus of these techniques has rightfully been identification and preservation of so-called "eloquent" brain functions (i.e., motor and language), but there is building momentum for more extensive mapping of cognitive and emotional networks. In addition, there is growing interest in mapping these functions in patients with a broad range of neurosurgical diseases. Resting-state functional MRI (rs-fMRI) is a noninvasive imaging modality that is able to measure spontaneous low-frequency blood oxygen level-dependent signal fluctuations at rest to infer neuronal activity. Rs-fMRI may be able to map cognitive and emotional networks for individual patients. In this review, the authors give an overview of the rs-fMRI technique and associated cognitive and emotional resting-state networks, discuss the potential applications of rs-fMRI, and propose future directions for the mapping of cognition and emotion in neurosurgical patients.

Characterization of postsurgical functional connectivity changes in temporal lobe epilepsy.

OBJECTIVE: Seizure outcome after mesial temporal lobe epilepsy (mTLE) surgery is complex and diverse, even across patients with homogeneous presurgical clinical profiles. The authors hypothesized that this is due in part to variations in network connectivity across the brain before and after surgery. Although presurgical network connectivity has been previously characterized in these patients, the objective of this study was to characterize presurgical to postsurgical functional network connectivity changes across the brain after mTLE surgery. METHODS: Twenty patients with drug-refractory unilateral mTLE (5 left side, 10 female, age 39.3 ± 13.5 years) who underwent either selective amygdalohippocampectomy (n = 13) or temporal lobectomy (n = 7) were included in the study. Presurgical and postsurgical (36.6 ± 14.3 months after surgery) functional connectivity (FC) was measured with 3-T MRI and compared with findings in age-matched healthy controls (n = 44, 21 female, age 39.3 ± 14.3 years). Postsurgical connectivity changes were then related to seizure outcome, type of surgery, and presurgical disease parameters. RESULTS: The results demonstrated significant decreases of FC from control group values across the brain after surgery that were not present before surgery, including many contralateral hippocampal connections distal to the surgical site. Postsurgical impairment of contralateral precuneus to ipsilateral occipital connectivity was associated with seizure recurrence. Presurgical impairment of the contralateral precuneus to contralateral temporal lobe connectivity was associated with those who underwent selective amygdalohippocampectomy compared to those who had temporal lobectomy. Finally, changes in thalamic connectivity after surgery were linearly related to duration of epilepsy and frequency of consciousness-impairing seizures prior to surgery. CONCLUSIONS: The widespread contralateral hippocampal FC changes after surgery may be a reflection of an ongoing epileptogenic progression that has been altered by the surgery, rather than a direct result of the surgery itself. This network evolution may contribute to long-term seizure outcome. Therefore, the combination of presurgical network mapping with the understanding of the dynamic effects of surgery on the networks may ultimately be used to create predictors of the likelihood of long-term seizure recurrence in individual patients after mTLE surgery.

Disconnection of the pathological connectome for multifocal epilepsy surgery.

OBJECTIVERecent neuroimaging studies suggest that intractable epilepsy involves pathological functional networks as well as strong epileptogenic foci. Combining cortico-cortical evoked potential (CCEP) recording and tractography is a useful strategy for mapping functional connectivity in normal and pathological networks. In this study, the authors sought to demonstrate the efficacy of preoperative combined CCEP recording, high gamma activity (HGA) mapping, and tractography for surgical planning, and of intraoperative CCEP measures for confirmation of selective pathological network disconnection.METHODSThe authors treated 4 cases of intractable epilepsy. Diffusion tensor imaging-based tractography data were acquired before the first surgery for subdural grid implantation. HGA and CCEP investigations were done after the first surgery, before the second surgery was performed to resect epileptogenic foci, with continuous CCEP monitoring during resection.RESULTSAll 4 patients in this report had measurable pathological CCEPs. The mean negative peak-1 latency of normal CCEPs related to language functions was 22.2 ± 3.5 msec, whereas pathological CCEP latencies varied between 18.1 and 22.4 msec. Pathological CCEPs diminished after complete disconnection in all cases. At last follow-up, all of the patients were in long-term postoperative seizure-free status, although 1 patient still suffered from visual aura every other month.CONCLUSIONSCombined CCEP measurement, HGA mapping, and tractography greatly facilitated targeted disconnection of pathological networks in this study. Although CCEP recording requires technical expertise, it allows for assessment of pathological network involvement in intractable epilepsy and may improve seizure outcome.

Electrocorticography and the early maturation of high-frequency suppression within the default mode network.

OBJECTIVE The acquisition and refinement of cognitive and behavioral skills during development is associated with the maturation of various brain oscillatory activities. Most developmental investigations have identified distinct patterns of low-frequency electrophysiological activity that are characteristic of various behavioral milestones. In this investigation, the authors focused on the cross-sectional developmental properties of high-frequency spectral power from the brain's default mode network (DMN) during goal-directed behavior. METHODS The authors contrasted regionally specific, time-evolving high gamma power (HGP) in the lateral DMN cortex between 3 young children (age range 3-6 years) and 3 adults by use of electrocorticography (ECoG) recordings over the left perisylvian cortex during a picture-naming task. RESULTS Across all participants, a nearly identical and consistent response suppression of HGP, which is a functional signature of the DMN, was observed during task performance recordings acquired from ECoG electrodes placed over the lateral DMN cortex. This finding provides evidence of relatively early maturation of the DMN. Furthermore, only HGP relative to evoked alpha and beta band power showed this level of consistency across all participants. CONCLUSIONS Regionally specific, task-evoked suppression of the high-frequency components of the cortical power spectrum is established early in brain development, and this response may reflect the early maturation of specific cognitive and/or computational mechanisms.

Functional connectivity analysis and prediction of cognitive change after carotid artery stenting.

OBJECTIVE: The neurocognitive course of patients who have undergone cerebral revascularization has been the subject of many studies, and the reported effects of carotid artery stenting (CAS) on cognitive function have varied from study to study. The authors hypothesized that cognitive amelioration after CAS is associated with alteration of the default mode network (DMN) connectivity, and they investigated the correlation between functional connectivity (FC) of the DMN and post-CAS changes in cognitive function in order to find a clinical marker that can be used to predict the effect of cerebral revascularization on patients' cognitive function in this preliminary exploratory study. METHODS: The authors examined post-CAS changes in cognitive function in relation to FC in patients treated for unilateral carotid artery stenosis. Resting-state functional MRI (rs-fMRI) was performed with a 3-T scanner before and 6 months after CAS in 8 patients. Neuropsychological tests (Wechsler Adult Intelligence Scale III and Wechsler Memory Scale-Revised) were administered to each patient before and 6 months after CAS. The DMN was mapped for each patient through independent component analysis of the rs-fMR images, and the correlation between FC of the DMN and post-CAS change in cognitive function was analyzed on a voxel level. Multivariable regression analysis was performed to identify preoperative factors associated with a post-CAS change in cognitive function. RESULTS: Post-CAS cognitive function varied between patients and between categories of neuropsychological tests. Although there was no significant overall improvement in Working Memory scores after CAS, post-CAS Working Memory scores changed in negative correlation with changes in FC between the DMN and the precentral/superior frontal gyrus and between the DMN and the middle frontal gyrus. In addition, the preoperative FC between those areas correlated positively with the post-CAS improvement in working memory. CONCLUSIONS: FC between the DMN and working memory-related areas is closely associated with improvement in working memory after CAS. Preoperative analysis of FC of the DMN may be useful for predicting postoperative improvement in the working memory of patients being treated for unilateral stenosis of the extracranial internal carotid artery.Clinical trial registration no.: UMIN000020045 (www.umin.ac.jp/ctr/index.htm).