Brain Plasticity and Reorganization Before, During, and After Glioma Resection

Historical Note

For more than 1 century, 2 different concepts of CNS functioning were suggested. First, the theory of equipotentiality hypothesized that the whole brain, or at least 1 complete hemisphere, was involved in the practice of a functional task. By contrast, in the theory of localizationism (based on phrenology), each part of the brain was supposed to correspond with a specific function. Progressively, an intermediate view emerged, namely a brain organized (1) in highly specialized functional areas, called eloquent regions (eg, the rolandic, Broca, and Wernicke areas), for which any lesion generates major permanent neurologic deficits; and (2) in noneloquent regions, with no functional consequences when damaged. Therefore, the dogma of a static CNS organization, with the inability to compensate for any damage involving the eloquent regions, was settled for a long time. Nevertheless, thanks to regular observations of functional improvement after injuries of structures considered as critical, this principle of a rigid CNS was called into question. If there is a lesion of neural tissue, the brain can reallocate the remaining physiologic resources to maintain a satisfactory level of function in a cognitively and socially demanding environment. Thus, many investigations were performed, initially in vitro and in animals, then more recently in humans, in order to study the mechanisms underlying these compensatory phenomena: the concept of neuroplasticity was developed. Advances in functional mapping and neuroimaging techniques have dramatically changed the classic modular model for a new dynamic and distributed perspective of CNS organization, able to reorganize itself both during everyday life (learning) and after a pathologic event such as a DG. However, although there are a few literature reports on cases of functional recovery or adaptation in various neurologic contexts, the most persuasive body of evidence for the brain's lesion-induced plasticity comes from neurosurgery in general and from the resection of DG in particular.

Definition and Mechanisms

Neuroplasticity is a continuous processing allowing short-term, medium-term, and long-term remodeling of the neuronosynaptic organization, with the aim of optimizing the functioning of neural networks during phylogenesis, ontogeny, and physiologic learning, and following brain injury. At a microscopic scale, pathophysiologic mechanisms underlying plasticity are mainly represented by synaptic efficacy modulations, unmasking of latent connections, phenotypic modifications, synchrony changes, and neurogenesis. At a macroscopic scale, diaschisis, functional redundancies, cross-modal plasticity with sensory substitution, and morphologic changes are involved. The behavioral consequences of these phenomena have been investigated, in particular the ability to recover after cerebral damage (postlesional plasticity), and the underlying patterns of functional remapping have been analyzed. Neural plasticity can be conceived only in a dynamic account of CNS organization; the brain is an ensemble of complex networks that form, reshape, and flush information dynamically. Thus, reorganization could occur, based on the existence of multiple and overlapping redundancies organized hierarchically. These findings have shown that neuronal aggregates, beside or outlying a lesion, can increasingly adopt the function of the damaged area and switch their own activation pattern to substitute the lesioned structure while facilitating functional recovery.

In this context, the concept of the brain connectome has recently emerged. This concept captures the characteristics of spatially distributed dynamic neural processes at multiple spatial and temporal scales. The new science of brain connectomics is contributing to both theoretic and computational models of the brain as a complex system, and experimentally to new indices and metrics (eg, nodes, hubs, efficiency, modularity) in order to characterize and scale the functional organization of the healthy and diseased CNS. However, in pathology, neural plasticity is possible only if the subcortical connectivity is preserved, to allow spatial communication and temporal synchronization among large interconnected networks, according to the principle of hodotopy. Although distinct patterns of subcortical plasticity were identified, namely unmasking of perilesional latent networks, recruitment of accessory pathways, introduction of additional relays within neuron-synaptic circuits, and involvement of parallel long-distance association pathways, the real capacity to build a new structural connectivity (so-called rewiring) leading to functional recovery have not yet been shown in humans.