The organization of basic functions of the human brain, particularly in the right hemisphere, remains poorly understood. Recent advances in functional neuroimaging have improved our understanding of cortical organization but do not allow for direct interrogation or determination of essential (versus participatory) cortical regions. Direct cortical stimulation represents a unique opportunity to provide novel insights into the functional distribution of critical epicentres. Direct cortical stimulation (bipolar, 60 Hz, 1-ms pulse) was performed in 165 consecutive patients undergoing awake mapping for resection of low-grade gliomas. Tasks included motor, sensory, counting, and picture naming. Stimulation sites eliciting positive (sensory/motor) or negative (speech arrest, dysarthria, anomia, phonological and semantic paraphasias) findings were recorded and mapped onto a standard Montreal Neurological Institute brain atlas. Montreal Neurological Institute-space functional data were subjected to cluster analysis algorithms (K-means, partition around medioids, hierarchical Ward) to elucidate crucial network epicentres. Sensorimotor function was observed in the pre/post-central gyri as expected. Articulation epicentres were also found within the pre/post-central gyri. However, speech arrest localized to ventral premotor cortex, not the classical Broca's area. Anomia/paraphasia data demonstrated foci not only within classical Wernicke's area but also within the middle and inferior frontal gyri. We report the first bilateral probabilistic map for crucial cortical epicentres of human brain functions in the right and left hemispheres, including sensory, motor, and language (speech, articulation, phonology and semantics). These data challenge classical theories of brain organization (e.g. Broca's area as speech output region) and provide a distributed framework for future studies of neural networks.
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.
Despite a better understanding of their anatomy, the functional role of frontal pathways, i.e., the fronto-striatal tract (FST) and frontal aslant tract (FAT), remains obscure. We studied 19 patients who underwent awake surgery for a frontal glioma (14 left, 5 right) by performing intraoperative electrical mapping of both fascicles during motor and language tasks. Furthermore, we evaluated the relationship between these tracts and the eventual onset of transient postoperative disorders. We also performed post-surgical tract-specific measurements on probabilistic tractography. All patients but one experienced intraoperative inhibition of movement and/or speech during subcortical electrostimulation. On postoperative tractography, the subcortical distribution of stimulated sites corresponded to the spatial course of the FST and/or FAT. Furthermore, we found a significant correlation between postoperative worsening and distances between these tracts and resection cavity. A resection close to the (right or left) FST was correlated with transitory motor initiation disorders (p = 0.026), while a resection close to the left FAT was associated with transient speech initiation disorders (p = 0.003). Moreover, the measurements of average distances between resection cavity and left FAT showed a positive correlation with verbal fluency in both semantic (p = 0.019) and phonemic scores (p = 0.017), while average distances between surgical cavity and left FST showed a positive correlation with verbal fluency scores in both semantic (p = 0.0003) and phonemic modalities (p = 0.037). We suggest that FST and FAT would cooperatively play a role in self-initiated movement and speech, as a part of "negative motor network" involving the pre-supplementary motor area, left inferior frontal gyrus and caudate nucleus.
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.
Consequential works in cognitive neuroscience have led to the formulation of an interactive dual-stream model of language processing: the dorsal stream may process the phonological aspects of language, whereas the ventral stream may process the semantic aspects of language. While it is well-accepted that the dorsal route is subserved by the arcuate fasciculus, the structural connectivity of the semantic ventral stream is a matter of dispute. Here we designed a longitudinal study to gain new insights into this central but controversial question. Thirty-one patients harboring a left diffuse low-grade glioma—a rare neurological condition that infiltrates preferentially white matter associative pathways—were assessed with a prototypical task of language (i.e. verbal fluency) before and after surgery. All were operated under local anesthesia with a cortical and subcortical brain mapping—enabling to identify and preserve eloquent structures for language. We performed voxel-based lesion-symptom (VLSM) analyses on pre- and postoperative behavioral data. Preoperatively, we found a significant relationship between semantic fluency scores and the white matter fibers shaping the ventro-lateral connectivity (P < 0.05 corrected). The statistical map was found to substantially overlap with the spatial position of the inferior fronto-occipital fasciculus (IFOF) (37.7%). Furthermore, a negative correlation was observed between semantic fluency scores and the infiltration volumes in this fasciculus (r = -0.4, P = 0.029). Postoperatively, VLSM analyses were inconclusive. Taken as a whole and when combined with the literature data, our findings strengthen the view that the IFOF plays an essential role in semantic processing and may subserve the direct ventral pathway of language.
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.
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