Neural Regeneration Research ›› 2024, Vol. 19 ›› Issue (5): 947-948.doi: 10.4103/1673-5374.382246

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Perspectives in human brain plasticity sparked by glioma invasion: from intraoperative (re)mappings to neural reconfigurations

Sam Ng, Hugues Duffau, Guillaume Herbet*#br#   

  1. Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France (Ng S, Duffau H, Herbet G)
    Institute of Functional Genomics, University of Montpellier, CNRS, INSERM, Montpellier, France (Ng S, Duffau H) 
    Praxiling Laboratory, UMR5267, CNRS, Paul Valéry- Montpellier 3 University, Montpellier, France (Herbet G)
  • Online:2024-05-15 Published:2023-10-31
  • Contact: Guillaume Herbet, PhD, guillaume.herbet@umontpellier.fr.

Abstract: Exploring the aptitude of the human brain to compensate functional consequences of a lesion damaging its structural architecture is a key challenge to improve patient care in various neurological diseases, to optimize neuroscientifically-informed strategies of postlesional rehabilitation, and ultimately to develop innovative neuro-regenerative therapies. The term ‘plasticity’, initially referring to the intrinsic propensity of neurons to modulate their synaptic transmission in a learning situation, was progressively transposed to brain injury research and clinical neurosciences. Indeed, in the event of brain damage, adaptive mechanisms of compensation allow a partial reshaping of the structure and activities of the central nervous system, thus permitting to some extent the maintenance of brain functions. Such findings have been observed in multiple clinical conditions, most notably in the context of diffuse low-grade gliomas (DLGGs) - a histopathological subgroup of slow-growing tumors that biologically integrates within the surrounding brain tissue, both at the synaptic (Venkatesh et al., 2019) and macro-structural levels (Numan et al., 2022). Contrary to acute neurological injuries such as stroke, where neurological recovery generally remains limited, patients with DLGGs can usually benefit from an extensive surgical excision without suffering from permanent neurological or cognitive deficits as long as critical neural structures are preserved thanks to modern intraoperative awake cognitive mapping (Lemaitre et al., 2022). Therefore, DLGGs may be viewed as a relevant model to grasp the neuroplastic mechanisms being deployed to counterbalance neuronal losses and to establish the neural fingerprints predictive of functional recovery in a lesion context. In this perspective article, the authors aimed to emphasize recent contributions investigating human brain plasticity in reaction to DLGG invasion. First, long-range axono-cortical connections are discussed as major substrates underlying spatial redeployments of brain functions. Second, the time-dependent and evolving aspects of cortical rewiring are reviewed in light of recent intraoperative direct electrical stimulation (DES) findings. Third, these spatiotemporal patterns are examined under the scope of global reconfigurations of the meta-networking brain, an emerging theory of brain functioning. Finally, a tentative dynamic and multilevel model of glioma-induced plasticity is proposed to pave the way to future research perspectives in the field.