Neuroplasticity: Insights from Patients Harboring Gliomas

Abstract

Neuroplasticity is the ability of the brain to reorganize itself during normal development and in response to illness. Recent advances in neuroimaging and direct cortical stimulation in human subjects have given neuroscientists a window into the timing and functional anatomy of brain networks underlying this dynamic process. This review will discuss the current knowledge about the mechanisms underlying neuroplasticity, with a particular emphasis on reorganization following CNS pathology. First, traditional mechanisms of neuroplasticity, most relevant to learning and memory, will be addressed, followed by a review of adaptive mechanisms in response to pathology, particularly the recruitment of perilesional cortical regions and unmasking of latent connections. Next, we discuss the utility and limitations of various investigative techniques, such as direct electrocortical stimulation (DES), functional magnetic resonance imaging (fMRI), corticocortical evoked potential (CCEP), and diffusion tensor imaging (DTI). Finally, the clinical utility of these results will be highlighted as well as possible future studies aimed at better understanding of the plastic potential of the brain with the ultimate goal of improving quality of life for patients with neurologic injury.

Figure 1

Mechanisms of neuroplasticity. Illustrated in panels (a)–(d) are the four primary mechanisms of neuroplasticity discussed in this review. (a) Plasticity hierarchy (adapted from Ius et al., 2011 [37]). Areas in green have a high potential for plasticity while areas in red have a low potential for plasticity. Three lesion examples are illustrated in this figure. A lesion in the anterior frontal cortex (orange) would likely exhibit a high plasticity potential due to its noncritical role in complex higher-order functions. Conversely, a lesion in the posterior superior temporal gyrus (yellow; Wernicke's area, a critical language network hub) or in the subcortical white matter tract (purple; inferior frontal occipital fasciculus, a major axonal pathway connecting receptive and expressive language areas) would be expected to have limited plasticity. (b) Cortical recruitment: when a cortical injury occurs (grey), perilesional synapses can be recruited to maintain synaptic integrity. (c) Cortical redundancy: redundant synapses are normally inhibited by interneurons (red shadow). Upon injury (grey), this inhibition is lost thus allowing for transmission of the redundant synapse. Instead of losing function, the redundant pathway compensates for the injured neurons. (d) Contralateral recruitment: a lesion (blue circle) in the hand motor area (green dashed region) can promote recruitment of the analogous contralateral hand area (green circle) to rescue hand function.

Figure 2

Neuroplasticity mapping methods. Illustrated in panels (a)–(d) are various brain mapping techniques performed on a 30-year-old right-handed male with low-grade glioma intraoperatively (a) and prior to surgery ((b)–(d)). The approximate tumor border is shown (red dash) in panels (b)–(d). (a) Postresection intraoperative photograph of functional sites elicited by direct electrical stimulation: tags B/C lip movement (yellow); tags E/F tongue movement (green); tag K speech difficulty (orange). Note the close correlation between cortical language (orange), lip motor (yellow), and tongue motor (green) sites obtained by fMRI (panel (b)). Other tags shown denote face motor sites. At the inferior/posterior border of the resection cavity, stimulation of the IFOF (gray asterisk) caused speech disturbance. (b) Functional MRI (fMRI) demonstrating language activation (green) at the junction of pars opercularis and precentral gyrus and lip (yellow) and tongue (green) motor activation in the inferior precentral gyrus. (c) Diffusion tensor imaging (DTI) demonstrating two major white matter bundles in close proximity to the tumor: the inferior frontal occipital fasciculus (IFOF, green) that transmits semantic language information and the corticospinal tract (CST, blue) which conveys descending primary motor information. (d) MRI-navigated transcranial magnetic stimulation (TMS) of the hand motor area of the precentral gyrus elicited overt muscle contraction.