Revisiting the Functional Anatomy of the Human Brain: Toward a Meta-Networking Theory of Cerebral Functions

Abstract

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 Based on these recent data on brain connectome, we challenge the traditional, outdated localizationist view and propose an alternative meta-networking theory.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.

Defining functional brain networks using unsupervised density-peak clustering

“…In sum, our findings add to a growing body of recent research on the functional organization of neural networks in the brain (Herbet and Duffau, 2020;Ipiña et al, 2019;Ji et al, 2019) by providing a framework for neuroscientists who are interested in explaining individual differences by examining the organization of brain networks. Figures Fig.…”

Can Non-invasive Brain Stimulation Be Considered to Facilitate Reoperation for Low-Grade Glioma Relapse by Eliciting Neuroplasticity?

“…In other words, the ultimate goal would be to change the respective weight of the nodes within a large-scale bilateral functional network, or even to modulate the interactions between brain systems-as it has been evidenced that language compensation after surgery for left LGG might involve non-language functions such as attentional resources, i.e., that picture naming recovery was correlated to the recruitment of the right frontoparietal attentional network (28). This means that such an innovative therapeutic strategy can be conceived only in a dynamic metanetworking account of neural processing, breaking with the traditional dogmatic localizationist theory (10); therefore, a stronger link should be built between cognitive neurosciences (as the new field of connectomics), technical advances in neuromodulation tools (as rTMS and tDCS), and elaboration of original management for glioma patients, based on a better understanding and guidance of interactions between tumor progression and brain adaptation. In this spirit, the next question could be to use NBS with the aim of catalyzing neuroplasticity and optimizing the extent of resection for gliomas involving critical neural networks even before the first surgery.…”

“…In fact, mechanisms of neuroplasticity induced by the slow progression of the LGG over the years, explaining why the vast majority of patients do experience only mild (or even no) neurological deficits at diagnosis (usually made because of inaugural seizures), open the door to massive surgical resection in areas deemed to be inoperable in a rigid localizationist view of brain processing, with functional recovery and return to a normal life (6)(7)(8)(9). Such a considerable functional redeployment is possible, thanks to an actual meta-networking brain organization, based on dynamic interactions within and between neural circuits subserving sensorimotor, visuospatial, language, cognitive, emotional, and behavioral functions (10).…”

Network Neuroscience and the Adapted Mind: Rethinking the Role of Network Theories in Evolutionary Psychology

“…Primarily used in the context of awake brain surgery to individually map a patient's anatomo-functional architecture, direct electrical stimulation aids surgeons to maximize resection (usually for tumorological or epileptological reasons) while minimizing postoperative deficits, the main concern being sparing neural tissue that is essential to quality of life. Albeit invasive, direct electrical stimulation is widely regarded as a uniquely precise and reliable method to investigate brain organization, as the ability to disturb in real-time the activity within a system provides great insights into the role played by each of its components (De Schotten et al, 2005;Mandonnet et al, 2010;Desmurget et al, 2013;Duffau, 2015;Herbet and Duffau, 2020). This surgical technique has been used for 150 years to probe functional roles of cortical areas, first in animals (Fritsch and Hitzig, 1870), then in humans (Bartholow, 1874), and is now being employed to investigate the network organization of the brain by assessing causal links between cognitive functions and white matter tracts.…”