Functional Translocation of Broca's Area in a Low-Grade Left Frontal Glioma: Graph Theory Reveals the Novel, Adaptive Network Connectivity

Abstract

We describe frontal language reorganization in a 50–60 year-old right-handed patient with a low-grade left frontotemporal insular glioma. Pre-operative fMRI revealed robust activation in the left superior temporal gyrus (Wernicke Area, WA) and in the right inferior frontal gyrus (right anatomical homolog of Broca Area, BA). Intra-operative cortical stimulation of the left inferior frontal gyrus and adjacent cortices elicited no speech deficits, and gross total resection including the expected location of BA resulted in no speech impairment. We employed statistical inference methods to reconstruct the functional brain network and determined how different brain areas connect with one another. We found that the right homolog of the BA in this patient functionally connected to the same areas as the left BA in a typical healthy control. As opposed to the functional connection of the left BA in a healthy brain, the right BA did not connect directly with the left WA, but connected indirectly, mediated by the pre-Supplementary Motor Area and the Middle Frontal Gyrus. This case illustrates that pre-surgical fMRI may be used to identify atypical hemispheric language reorganization in the presence of brain tumor and that network theory opens the possibility for future insight into the neural mechanism underlying the language reorganization.

What do we know about pre- and postoperative plasticity in patients with glioma? A review of neuroimaging and intraoperative mapping studies

“…With regard to the language network, compensatory recruitment of perilesional areas was observed following tumor invasion of crucial areas including Broca’s area (e.g., Benzagmout et al, 2007 , Lubrano et al, 2010 , Thiel et al, 2001 ; for single cases, see Chan et al, 2019 , De Benedictis et al, 2012 , Meyer et al, 2003a , Plaza et al, 2009 ), perisylvian regions such as Wernicke’s area ( Ille et al, 2019 ; Thiel et al, 2001 ), and the left insula (e.g., Duffau et al, 2006 ; for single cases, see Duffau et al, 2001 , Li et al, 2019 ). A limited but feasible perilesional compensatory activation was also observed for the premotor cortex, which also supports language functions (e.g., Gil Robles et al, 2008 ).…”

“…Interestingly, several single-case studies reported preoperative translocation of either Broca’s (e.g., Holodny et al, 2002 , Li et al, 2019 ) or Wernicke’s area (e.g., Petrovich et al, 2004 ), even though the other non-affected area was still active in the left (language-dominant) hemisphere. Notably, this reorganization then enabled total resection of the no-longer functional left area, without causing permanent language deficits.…”

“…A few studies investigated functional connectivity changes in relation to language. Li et al (2019) described the successful adaptive connectivity remodeling in a patient with a left fronto-temporo-insular LGG. In detail, activation of Broca’s area was recorded in the right hemisphere, whereas Wernicke’s area still activated in the affected hemisphere.…”

Improving brain health by identifying structure-function relations in patients with neurosurgical disorders

“…The high incidence of postoperative cognitive decline in patients with low grade glioma could be explained by some functional activity remaining within the tumour mass. 18 Focal brain tumours produce global changes in the functionally complex and networked brain architecture, which may aid in our understanding of patients' larger scale Intraoperative neurophysiological monitoring refers to a group of procedures used to monitor neural pathways during high risk operations to help surgeons avoid damage to the nervous system. It includes techniques to identify impending damage and techniques to map the vital structures of the nervous system Awake brain surgery (awake craniotomy) is a neurosurgical technique that allows a surgeon to remove the tumour or epileptic tissue while the patient is awake to avoid brain damage.…”

“…The high incidence of postoperative cognitive decline in patients with low grade glioma could be explained by some functional activity remaining within the tumour mass. 18 Focal brain tumours produce global changes in the functionally complex and networked brain architecture, which may aid in our understanding of patients’ larger scale neurological manifestations and provide a framework for improving plasticity. 19 Of note, recent reports have linked neuronal excitability with growth of gliomas and brain metastases.…”