Pathological Neural Attractor Dynamics in Slowly Growing Gliomas Supports an Optimal Time Frame for White Matter Plasticity

Abstract

Neurological function in patients with slowly growing brain tumors can be preserved even after extensive tumor resection. However, the global process of cortical reshaping and cerebral redistribution cannot be understood without taking into account the white matter tracts. The aim of this study was to predict the functional consequences of tumor-induced white matter damage by computer simulation. A computational model was proposed, incorporating two cortical patches and the white matter connections of the uncinate fasciculus. Tumor-induced structural changes were modeled such that different aspects of the connectivity were altered, mimicking the biological heterogeneity of gliomas. The network performance was quantified by comparing memory pattern recall and the plastic compensatory capacity of the network was analyzed. The model predicts an optimal level of synaptic conductance boost that compensates for tumor-induced connectivity loss. Tumor density appears to change the optimal plasticity regime, but tumor size does not. Compensatory conductance values that are too high lead to performance loss in the network and eventually to epileptic activity. Tumors of different configurations show differences in memory recall performance with slightly lower plasticity values for dense tumors compared to more diffuse tumors. Simulation results also suggest an optimal noise level that is capable of increasing the recall performance in tumor-induced white matter damage. In conclusion, the model presented here is able to capture the influence of different tumor-related parameters on memory pattern recall decline and provides a new way to study the functional consequences of white matter invasion by slowly growing brain tumors.

Diffuse low-grade gliomas and neuroplasticity

“…This is occasionally seen in the short term as the resection proceeds [55]. In addition, wide resections, particularly if complete on imaging, improve control of the epilepsy in approximately 80% of cases, particularly in patients with prolonged preoperative epilepsy, which again may improve the plasticity potential, as the seizures have been modeled as a limitation to neuroplasticity [63]. In addition, progression of the residual DLGG probably helps to continue to trigger map remodeling, a process which was already ongoing before the surgery.…”

“…These results have led to the recent proposal for a routine MR screening policy in a selected group of the general population (particularly young adults) [86]. As the risk of causing postoperative functional problems is minimal and the likelihood of complete or even supratotal resection is optimized in asymptomatic patients (as the tumor volume is lower), this approach is wholly justified [87] particularly as the potential for plasticity has not yet reached its limit, as by definition no epileptic seizures have yet developed [63].…”

Similarities and differences in neuroplasticity mechanisms between brain gliomas and nonlesional epilepsy

“…Differences in the degree of plasticity according to the nature of brain damage could probably be explained by neurobiologic mechanisms. Regarding tumor surgery, more and more data are now available regarding these neurobiologic mechanisms, and computational models involving different types of brain tumors have shown that tumor cell density rather than tumor size was the crucial factor …”

“…Regarding tumor surgery, more and more data are now available regarding these neurobiologic mechanisms, and computational models involving different types of brain tumors have shown that tumor cell density rather than tumor size was the crucial factor. 82 Regarding nonlesional and malformative epilepsy, we previously showed that the absence of tumor, which would trigger neuroplasticity, explains why no functional reorganization occurs in the neocortex. Epilepsy duration is known to be a major factor of bad seizure outcome in epilepsy surgery.…”

Atypical crossmodal emotional integration in patients with gliomas

“…LGG show a continuous, constant growth (about 4 mms/year) in local, white matter and systematically evolve toward HGG (Bonnetblanc, Desmurget, & Duffau, 2006), with a median of around 7-8 years for anaplastic transformation and a median survival around 10 years without treatment (Duffau, 2005). Due to their slow development and infiltrating characteristics, gliomas efficiently activate brain plasticity and connectivity (Duffau, Capelle, & Denvil, 2003;Szalisznyo, Silverstein, Duffau, & Smits, 2013).…”