For more than one century, brain processing was mainly thought in a localizationist framework, in which one given function was underpinned by a discrete, isolated cortical area, and with a similar ...cerebral organization across individuals. However, advances in brain mapping techniques in humans have provided new insights into the organizational principles of anatomo-functional architecture. Here, we review recent findings gained from neuroimaging, electrophysiological, as well as lesion studies. Based on these recent data on brain connectome, we challenge the traditional, outdated localizationist view and propose an alternative meta-networking theory. This model holds that complex cognitions and behaviors arise from the spatiotemporal integration of distributed but relatively specialized networks underlying conation and cognition (e.g., language, spatial cognition). Dynamic interactions between such circuits result in a perpetual succession of new equilibrium states, opening the door to considerable interindividual behavioral variability and to neuroplastic phenomena. Indeed, a meta-networking organization underlies the uniquely human propensity to learn complex abilities, and also explains how postlesional reshaping can lead to some degrees of functional compensation in brain-damaged patients. We discuss the major implications of this approach in fundamental neurosciences as well as for clinical developments, especially in neurology, psychiatry, neurorehabilitation, and restorative neurosurgery.
Historically, the study of patients with spatial neglect has provided fundamental insights into the neural basis of spatial attention. However, lesion mapping studies have been unsuccessful in ...establishing the potential role of associative networks spreading on the dorsal-medial axis, mainly because they are uncommonly targeted by vascular injuries. Here we combine machine learning-based lesion-symptom mapping, disconnection analyses and the longitudinal behavioral data of 128 patients with well-delineated surgical resections. The analyses show that surgical resections in a location compatible with both the supplementary and the cingulate eye fields, and disrupting the dorsal-medial fiber network, are specifically associated with severely diminished performance on a visual search task (i.e., visuo-motor exploratory neglect) with intact performance on a task probing the perceptual component of neglect. This general finding provides causal evidence for a role of the frontal-medial network in the voluntary deployment of visuo-spatial attention.
The inferior longitudinal fasciculus (ILF) is a long-range, associative white matter pathway that connects the occipital and temporal-occipital areas of the brain to the anterior temporal areas. In ...view of the ILF's anatomic connections, it has been suggested that this pathway has a major role in a relatively large array of brain functions. Until recently, however, the literature data on these potential functions were scarce. Here, we review the key findings of recent anatomic, neuromodulation, and neuropsychological studies. We also summarize reports on how this tract is disrupted in a wide range of brain disorders, including psychopathologic, neurodevelopmental, and neurologic diseases. Our review reveals that the ILF is a multilayered, bidirectional tract involved in processing and modulating visual cues and thus in visually guided decisions and behaviors. Accordingly, sudden disruption of the ILF by neurologic insult is mainly associated with neuropsychological impairments of visual cognition (e.g., visual agnosia, prosopagnosia, and alexia). Furthermore, disruption of the ILF may constitute the pathophysiologic basis for visual hallucinations and socio-emotional impairments in schizophrenia, as well as emotional difficulties in autism spectrum disorder. Degeneration of the ILF in neurodegenerative diseases affecting the temporal lobe may explain (at least in part) the gradual onset of semantic and lexical access difficulties. Although some of the functions mediated by the ILF appear to be relatively lateralized, observations from neurosurgery suggest that disruption of the tract's anterior portion can be dynamically compensated for by the contralateral portion. This might explain why bilateral disruption of the ILF in either acute or progressive disease is highly detrimental in neuropsychological terms.
It is increasingly acknowledged that the brain is highly plastic. However, the anatomic factors governing the potential for neuroplasticity have hardly been investigated. To bridge this knowledge ...gap, we generated a probabilistic atlas of functional plasticity derived from both anatomic magnetic resonance imaging results and intraoperative mapping data on 231 patients having undergone surgery for diffuse, low-grade glioma. The atlas includes detailed level of confidence information and is supplemented with a series of comprehensive, connectivity-based cluster analyses. Our results show that cortical plasticity is generally high in the cortex (except in primary unimodal areas and in a small set of neural hubs) and rather low in connective tracts (especially associative and projection tracts). The atlas sheds new light on the topological organization of critical neural systems and may also be useful in predicting the likelihood of recovery (as a function of lesion topology) in various neuropathological conditions-a crucial factor in improving the care of brain-damaged patients.
Accessing the meaning of words, objects, people and facts is a human ability, made possible thanks to semantic processing. Although studies concerning its cortical organization are proficient, the ...subcortical connectivity underlying this semantic network received less attention.
We used intraoperative direct electrostimulation, which mimics a transient virtual lesion during brain surgery for glioma in eight awaken patients, to map the anatomical white matter substrate subserving the semantic system. Patients performed a picture naming task and a non-verbal semantic association test during the electrical mapping.
Direct electrostimulation of the inferior fronto-occipital fascicle, a poorly known ventral association pathway which runs throughout the brain, induced in all cases semantic disturbances. These transient disorders were highly reproducible, and concerned verbal as well as non-verbal output.
Our results highlight for the first time the essential role of the left inferior fronto-occipital fascicle in multimodal (and not only in verbal) semantic processing. On the basis of these original findings, and in the lights of phylogenetic considerations regarding this fascicle, we suggest its possible implication in the monitoring of the human level of consciousness related to semantic memory, namely noetic consciousness.
•Direct electrical stimulation of the left IFOF induces semantic disorders.•The left IFOF sub serves both verbal and non-verbal semantic processing in humans.•The left IFOF constitutes the irreplaceable ventral stream of the semantic system.•The left IFOF might be involved in the properly human “noetic consciousness”.
The structural and functional organization of brain networks subserving basic daily activities (i.e. language, visuo-spatial cognition, movement, semantics, etc.) are not completely understood to ...date. Here, we report the first probabilistic cortical and subcortical atlas of critical structures mediating human brain functions based on direct electrical stimulation (DES), a well-validated tool for the exploration of cerebral processing and for performing safe surgical interventions in eloquent areas.
We collected 1162 cortical and 659 subcortical DES responses during testing of 16 functional domains in 256 patients undergoing awake surgery. Spatial coordinates for each functional response were calculated, and probability distributions for the entire patient cohort were mapped onto a standardized three-dimensional brain template using a multinomial statistical analysis. In addition, matching analyses were performed against prior established anatomy-based cortical and white matter (WM) atlases.
The probabilistic maps for each functional domain were provided. The topographical analysis demonstrated a wide spatial distribution of cortical functional responses, while subcortical responses were more restricted, localizing to known WM pathways. These DES-derived data showed reliable matching with existing cortical and WM atlases as well as recent neuroimaging and neurophysiological data.
We present the first integrated and comprehensive cortical-subcortical atlas of structures essential for humans’ neural functions based on highly-specific DES mapping during real-time neuropsychological testing. This novel atlas can serve as a complementary tool for neuroscientists, along with data obtained from other modalities, to improve and refine our understanding of the functional anatomy of critical brain networks.
•1821 direct electrical stimulation sites from 256 awake brain surgeries analyzed.•Probability maps of 16 key human brain functions generated.•Cortical stimulation points widely distributed over the brain surface.•Subcortical responses more restricted, localize to known major white matter tracts.
The neural foundations underlying semantic processing have been extensively investigated, highlighting a pivotal role of the ventral stream. However, although studies concerning the involvement of ...the left ventral route in verbal semantics are proficient, the potential implication of the right ventral pathway in non-verbal semantics has been to date unexplored. To gain insights on this matter, we used an intraoperative direct electrostimulation to map the structures mediating the non-verbal semantic system in the right hemisphere. Thirteen patients presenting with a right low-grade glioma located within or close to the ventral stream were included. During the ‘awake’ procedure, patients performed both a visual non-verbal semantic task and a verbal (control) task. At the cortical level, in the right hemisphere, we found non-verbal semantic-related sites (
n
= 7 in 6 patients) in structures commonly associated with verbal semantic processes in the left hemisphere, including the superior temporal gyrus, the pars triangularis, and the dorsolateral prefrontal cortex. At the subcortical level, we found non-verbal semantic-related sites in all but one patient (
n
= 15 sites in 12 patients). Importantly, all these responsive stimulation points were located on the spatial course of the right inferior fronto-occipital fasciculus (IFOF). These findings provide direct support for a critical role of the right IFOF in non-verbal semantic processing. Based upon these original data, and in connection with previous findings showing the involvement of the left IFOF in non-verbal semantic processing, we hypothesize the existence of a bilateral network underpinning the non-verbal semantic system, with a homotopic connectional architecture.
For many years, the right hemisphere (RH) was considered as nondominant, especially in right-handers. In neurosurgical practice, this dogma resulted in the selection of awake procedure with language ...mapping only for lesions of the left dominant hemisphere. Conversely, surgery under general anesthesia (possibly with motor mapping) was usually proposed for right lesions. However, when objective neuropsychological assessments were performed, they frequently showed cognitive and behavioral deficits after brain surgery, even in the RH. Therefore, to preserve an optimal quality of life, especially in patients with a long survival expectancy (as in low-grade gliomas), awake surgery with cortical and axonal electrostimulation mapping has recently been proposed for resection of right tumors. Here, we review new insights gained from intraoperative stimulation into the pivotal role of the RH in movement execution and control, visual processes and spatial cognition, language and nonverbal semantic processing, executive functions (e.g., attention), and social cognition (mentalizing and emotion recognition). These original findings, which break with the myth of a nondominant RH, may have important implications in cognitive neurosciences, by improving our knowledge of the functional connectivity of the RH, as well as for the clinical management of patients with a right lesion. In brain surgery, awake mapping should be considered more systematically in the RH. Moreover, neuropsychological examination must be achieved in a more systematic manner before and after surgery within the RH, to optimize care by predicting the likelihood of functional recovery and by elaborating specific programs of rehabilitation.
Over the past few years, considerable progress has been done in clarifying the neural networks underlying mentalizing. However, although the cortical architecture of this function is relatively well ...understood, the white matter pathways that may be involved in conveying neural signals within the mentalizing network remain to be elucidated. To gain insight into this matter, a detailed stimulation mapping of face-based mentalizing was performed in 27 patients undergoing awake surgery for a right-sided diffuse low-grade glioma (DLGG). Direct electrical stimulation (DES) was applied to both the cortical and subcortical levels. In perfect agreement with previous literature using face-based mentalizing tasks, cortical sites were identified in the posterior inferior frontal gyrus (IFG), the dorsolateral prefrontal cortex (dlPFC), and the posterior superior temporal gyrus (pSTG). Most importantly, critical sites were found along the inferior fronto-occipital fasciculus (IFOF), and within the white matter fibres supplying the dlPFC. Disconnectome analyses confirmed the very high probability of IFOF disconnection during temporal subcortical stimulation, and revealed an additional implication of the superior longitudinal fasciculus/arcuate fasciculus (SLF/AF) during prefrontal subcortical stimulations. Altogether, these findings suggest that functional integrity of both the IFOF and the SLF is required for accurately inferring complex mental states from human faces.
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