Connectomics as a prognostic tool of functional outcome in glioma surgery of the supplementary motor area: illustrative case

Eric Suero Molina Computational NeuroSurgery (CNS) Lab, Macquarie Medical School, Faculty of Medicine, Health and Human Science, Macquarie University, Sydney, Australia
Macquarie Neurosurgery, Macquarie University Hospital, Sydney, Australia
Department of Neurosurgery, University Hospital of Münster, Münster, Germany; and

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Matthew J. Tait Macquarie Neurosurgery, Macquarie University Hospital, Sydney, Australia
Department of Neurosurgery, Nepean Public Hospital, Sydney, Australia

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Antonio Di Ieva Computational NeuroSurgery (CNS) Lab, Macquarie Medical School, Faculty of Medicine, Health and Human Science, Macquarie University, Sydney, Australia
Macquarie Neurosurgery, Macquarie University Hospital, Sydney, Australia

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BACKGROUND

The supplementary motor area (SMA) is essential in facilitating the commencement and coordination of complex self-initiated movements. Its complex functional connectivity poses a great risk for postoperative neurological deterioration. SMA syndrome can occur after tumor resection and comprises hemiakinesia and akinetic mutism (often, but unpredictably temporary). Although awake surgery is preferred for mapping and monitoring eloquent areas, connectomics is emerging as a novel technique to tailor neurosurgical approaches and predict functional prognosis, as illustrated in this case.

OBSERVATIONS

The authors report on a patient presenting with recurrent oligodendroglioma after subtotal resection 7 years earlier. After extensive neuropsychological and neuroradiological assessment (including connectomics), awake surgery was indicated. No intraoperative deficits were recorded; however, the patient presented with postoperative right-sided akinesia and mutism. Postoperative neuroimaging demonstrated the connectome overlapping the preoperative one, and indeed, neurological symptoms resolved after 3 days.

LESSONS

Comparison of the pre- and postoperative connectome can be used to objectively evaluate surgical outcomes and assess patient prognosis. To the best of the authors’ knowledge, this is the first case demonstrating the feasibility of quantitative functional connectivity analysis as a prognostic tool for neurological improvement after surgery. A better understanding of brain networks is instrumental for improving diagnosis, prognosis, and treatment of neuro-oncological patients.

ABBREVIATIONS

ATRX = Alpha thalassemia X-linked intellectual disability; DTI = diffuse tensor imaging; DWI = diffusion-weighted imaging; FAT = frontal aslant tract; FOV = field of view; HCP = Human Connectome Project; ML = machine learning; MRI = magnetic resonance imaging; rs-fMRI = resting-state functional MRI; SMA = supplementary motor area; TE = echo time; TR = repetition time

BACKGROUND

The supplementary motor area (SMA) is essential in facilitating the commencement and coordination of complex self-initiated movements. Its complex functional connectivity poses a great risk for postoperative neurological deterioration. SMA syndrome can occur after tumor resection and comprises hemiakinesia and akinetic mutism (often, but unpredictably temporary). Although awake surgery is preferred for mapping and monitoring eloquent areas, connectomics is emerging as a novel technique to tailor neurosurgical approaches and predict functional prognosis, as illustrated in this case.

OBSERVATIONS

The authors report on a patient presenting with recurrent oligodendroglioma after subtotal resection 7 years earlier. After extensive neuropsychological and neuroradiological assessment (including connectomics), awake surgery was indicated. No intraoperative deficits were recorded; however, the patient presented with postoperative right-sided akinesia and mutism. Postoperative neuroimaging demonstrated the connectome overlapping the preoperative one, and indeed, neurological symptoms resolved after 3 days.

LESSONS

Comparison of the pre- and postoperative connectome can be used to objectively evaluate surgical outcomes and assess patient prognosis. To the best of the authors’ knowledge, this is the first case demonstrating the feasibility of quantitative functional connectivity analysis as a prognostic tool for neurological improvement after surgery. A better understanding of brain networks is instrumental for improving diagnosis, prognosis, and treatment of neuro-oncological patients.

ABBREVIATIONS

ATRX = Alpha thalassemia X-linked intellectual disability; DTI = diffuse tensor imaging; DWI = diffusion-weighted imaging; FAT = frontal aslant tract; FOV = field of view; HCP = Human Connectome Project; ML = machine learning; MRI = magnetic resonance imaging; rs-fMRI = resting-state functional MRI; SMA = supplementary motor area; TE = echo time; TR = repetition time

Resection of intra-axial tumors of the medial frontal lobe can cause the so-called supplementary motor area (SMA) syndrome. This syndrome is often transitory and can involve mild hypokinesis aggravating up to hemiakinesia with muscle tone retention. When the dominant hemisphere is affected, speech hesitancy and akinetic mutism can also occur.1,2 The SMA is also involved in timing of and coordinating bilateral sequential extremity actions,3,4 as well as in the coordination of externally prompted motor actions (e.g., grasping visual objects).5 The etiology behind the SMA syndrome is an ongoing discussion. Until recently, injury to the posteromedial bank of the superior frontal gyrus was believed to be the leading cause of this neurological impairment. However, as connectomics research of the human brain is shifting how we evaluate surgical morbidity and treatment strategies, a network-based approach might be more likely to elucidate the reason behind this syndrome. The assessment of the risk related to the injury of brain networks and their connectivity could shift neurosurgeons toward connectome-based approaches. Moreover, the comparison of pre- and postoperative connectomics could also be related to functional prognostication, as illustrated here.

Illustrative Case

A right-handed 41-year-old female presented with a growing remnant of a glioma in the left frontal gyrus, within the SMA, after having undergone surgery 7 years earlier by another neurosurgeon (diagnosis: oligodendroglioma grade 2, isocitrate dehydrogenase 1 [IDH1]–mutant, 1p/19q-codeleted, ATRX retained, with rare single cells weakly positive for p53, and KI-67 <5%). Radiological follow-up over time showed progressive growth of the remnant (Fig. 1), although no further treatment had been offered.

FIG. 1.
FIG. 1.

Preoperative coronal fluid-attenuated inversion recovery (FLAIR) magnetic resonance imaging (MRI) (A) and axial 18F-fluorethyl-l-tyrosine positron emission tomography (18F-FET PET)–computed tomography (B) demonstrating growth of the known remnant with no high 18F-FET uptake, suspicious for recurrence of the previously resected oligodendroglioma grade 2. Coronal diffuse tensor imaging (DTI) and resting-state functional MRI (rs-fMRI) (C) merged together on Quicktome software, potentially showing some disruption of the frontal aslant tract (FAT) (white arrow).

A few transitory episodes of weakness in the right hand led the patient to seek a second opinion at our institute. On neurological testing, her function was essentially unremarkable. After extensive neuropsychological, neurological, and neuroradiological assessments, consensus was sought within the institute’s neuro-oncology multidisciplinary team meeting, and awake surgery was indicated. To perform supramaximal resection of the glioma and to preserve the patient’s neurological function, preoperative connectome analysis was performed. The latter was achieved by acquiring diffusion tensor imaging (DTI) and resting-state functional magnetic resonance imaging (rs-fMRI).

Diffusion-weighted imaging (DWI) parameters were as follows: slice thickness = 5 mm, field of view (FOV) = 220 × 220 mm, matrix = 128 × 128 mm, repetition time (TR) = 6000 ms, echo time (TE) = 114 ms, 64 diffusion directions with b-value = 1000 s/mm2, and 1 image with no diffusion weighting (b = 0 s/mm2). Acquisition time was 12 minutes. An rs-fMRI scan was acquired as a T2-star echo planar imaging sequence with 3 × 3 × 3–mm voxels, 128 volumes/run, TE = 27 ms, TR = 2.8 ms, FOV = 256 mm, flip angle = 90°, and acquisition time of 12 minutes.

The DWI and rs-fMRI data were processed using Quicktome and Infinitome software (Omniscient Neurotechnology),6 which uses a machine learning (ML) approach to model the diagnostic group of a single participant based on the pairwise functional correlation between the 379 regions of each individual’s brain atlas. The Pearson correlation coefficient was calculated between the blood oxygen level–dependent signals of each unique area pair. The patient’s functional connectivity was compared with the publicly available imaging data from the Human Connectome Project (HCP). The Omniscient software creates an ML-based, subject-specific version of the HCP Multimodal Parcellation (version 1.0, http://humanconnectome.org) based on structural connectivity data from 1200 healthy subjects.

In our case, impairment of the frontal aslant tract (FAT) was depicted on DTI (Fig. 1C), eventually related to the tumor and previous surgery, and eventually justifying impaired connectivity in the salience network.

Asleep-awake-asleep surgery was offered and performed under continuous neuromonitoring. During surgery, bipolar stimulation of the posterior portion of the middle frontal gyrus at 5 mA caused intraoperative seizures that were quickly controlled with iced water. The superior frontal gyrus was mapped without recognition of an eloquent area while performing various ideo-motor skill tests (assessed intraoperatively by a neuropsychologist), including object manipulation. Once the medial and lateral surgical margins were identified, the resection was continued dorsally until the corticospinal tract was stimulated at a minimum of 3 mA, representing a margin of at least 3 mm from the eloquent motor area. After the resection margins were identified, subpial resection under continuous subcortical monitoring was performed. No neurological deficits were triggered by stimulating and resecting the medial and lateral margins of the tumor, nor the posterolateral margins, while the posteromedial one was confirmed to be 2 mm adjacent to the corticospinal tract. Therefore, the apparent posterior anatomical margin was resected supramaximally in its lateral part but not in its medial components (avoiding the preoperatively planned supramaximal resection only on that area). Medially, the cingulum was reached and preserved, preserving subpially the callosal margin artery. The corpus callosum was also reached, leaving it intact (its stimulation caused a motor response of the left hand; Fig. 2).

FIG. 2.
FIG. 2.

Intraoperative neuro-navigation (Brainlab AG) showed supramaximal resection beyond the anterior (A), medial (B), posterosuperior (C), and posterolateral (D) edges of the tumor but not in its posteromedial (E) edge, which was adjacent to functional corticospinal tract, as shown on intraoperative neuromonitoring.

Supramaximal resection was achieved in a seemingly safe fashion from both a neurological and neurophysiological point of view. Before putting the patient asleep again for final hemostasis and closure, the patient was checked one last time. She showed no deficits, with normal speech response, normal cognitive functions, and normal strength in her 4 limbs.

Histopathological analysis confirmed the diagnosis of recurrent oligodendroglioma grade 2, with no evidence of grade progression and with overlapping features when compared with the previous surgical sample (although with slightly less cellularity and lower proliferation, as well as patchy microcystic changes and scant siderophages). Despite normal neurological function during the awake part of the operation and normal neuromonitoring (including somatosensory and motor-evoked potentials) after skin closure, surprisingly, the patient experienced postoperative akinetic mutism and dense right-sided hemiplegia. Postoperative magnetic resonance imaging (MRI) demonstrated that supramaximal resection had been achieved (volumetric analysis confirmed ∼115% resection of the presurgical tumor volume) with no signs of impaired restriction and a small amount of blood products along the resection cavity (Fig. 3), which eventually resolved at the neuroradiological follow-up 3 months after the operation.

FIG. 3.
FIG. 3.

Postoperative axial T1 FLAIR (A) and coronal T2-weighted (B) imaging demonstrating complete resection/supramaximal resection of the oligodendroglioma recurrence in all but the posterior margin, with some minor surgical changes and blood products along the medial resection cavity. There was no sign of stroke (no restrictions on diffusion-weighted imaging; not shown in the figure).

Imaging for connectomics was performed again (the day after the resection) and compared with the preoperative data with particular attention to the anatomical integrity of the tracts and functional preservation of the brain networks adjacent to the surgical cavity. No apparent disconnection of the important associative fibers or functional impairment was identified, indicating a good prognosis for potential neurological recovery (Figs. 4 and 5).

FIG. 4.
FIG. 4.

Postoperative DTI and connectome imaging showing very close proximity of the surgical cavity to the sensorimotor (A), salience (B), and language (C) network parcellations, without any apparent structural and functional impairment of these networks.

FIG. 5.
FIG. 5.

Pre- and postoperative quantitative anomaly matrices of the sensorimotor network of the patient compared with normative matrices generated from 200 healthy adults (A). No relevant difference could be observed between the preoperative (B) and postoperative (C) matrices of the patient, potentially confirming anatomical and functional preservation of this network (no differences were found in the other networks, including the language ones; not shown in the figure).

The patient’s symptoms subsequently resolved quickly. Resolution of the akinetic mutism occurred after 3 days, and strength on the right side of the patient’s body returned to normal power after 6 days. At 2 years’ follow-up, the patient remained neurologically intact and did not demonstrate any tumor recurrence.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

Although it is difficult to depict the underlying reason for the postoperative impairment in this patient, postoperative MRI showed intact associative fibers and functional networks around the surgical cavity, with no pruning of the structural connection or the main nodes forming the functional hubs. According to these results, good functional recovery in a few days was predicted, and the patient and her family were consulted (and reassured) accordingly. Deciding on the correct strategy to treat SMA tumors remains complex. The dogma of glioma surgery is to achieve maximal resection while keeping the patient safe. Thus, finding the optimal onco-functional balance remains the highest priority for treating patients with glioma.

Of 180 brain parcellations described in the Glasser et al. study,7 4 were involved in the SMA8: the superior frontal language area, Brodmann area 6 medial anterior, Brodmann area 6 medial parietal, and the supplementary and cingulate eye field. The SMA is connected with the ipsi- and contralateral premotor areas for initiating movement. Its complex connectivity is resembled not only by the different parcellations involved but also by the numerous interconnections with the insula, the anterior cingulate cortex, and the cerebellum, to name a few.9

A further important connection pathway provides the FAT, a white matter tract connecting the SMA, with the prefrontal cortex.10 Goulden et al.11 showed that the FAT mediates between the main hubs of the salience network. This cingulo-insular-opercular axis has been established to facilitate the shift between internal and external cognitive processes, a feature of the SMA syndrome in which patients cannot effectuate desired actions.12

Evidence suggests that the FAT acts as a central pathway between the SMA and both the premotor areas and area 44, which is the principal Broca area for speech production,12–14 explaining its involvement in mutism. Impairment of the FAT may justify a disconnection of the salience network and then a diffuse impairment in the prefrontal cognitive axis, formed by the default mode network connected via the cingulum, the salience network, and the SMA, which takes a crucial position as an important connectivity hub.15 Any impairment in the SMA (e.g., from a tumor and/or surgery) could impair the functional network related to the execution of movements and goal-directed behavior. Preserving the FAT seems paramount to avoid the SMA syndrome,12 and surgical approaches should be tailored to avoid crossing the FAT. In our patient, the FAT was already potentially impaired but not completely damaged, making it and the whole network related to it more susceptible to injury and then making the patient more prone to postoperative neurological dysfunction. Our case also confirms the recent observation that oligodendrogliomas tend to infiltrate the FAT, as compared with astrocytomas, which eventually tend to displace it.16 Patterns of cortical rearrangement of the underlying networks occurring after the first resection in this patient should also be considered, according to the well-demonstrated neuroplasticity occurring after diffuse low-grade glioma surgery.17 This explains the ability of the brain to adjust its networks in reaction to experience or cognition, which assists in maintaining optimal interaction levels with the internal or external stimuli.18,19

Because of their slow growth, low-grade gliomas have been good subjects for the investigation of neuroplasticity in tumors.20 The interplay between glioma cells and their local environment promotes neural circuit integration and network reorganization,21,22 resulting in neuroplastic modulations that could explain the relatively low neurological or cognitive impairments observed in patients with low-grade glioma before and after the resection of areas typically or formerly considered as “eloquent.”17,23

A “crossed” FAT has also been described as a white matter tract that connects the SMA with the contralateral premotor area and SMA through the corpus callosum. This pathway explains bilateral hand-movement coordination of the SMA8,24 and is suspected to be involved in neurological recovery during and after a temporary SMA syndrome. Compensation from the opposite hemisphere is a theory reinforced by research on functional connectivity,25 with several studies reporting a surge in the level of activity of the contralateral SMA26,27 when preserving the crossed FAT fibers.12

The SMA is thus an intricate and highly functional brain region. Primate studies28 initially provided insight into its functional connectivity. More recently, the field of connectomics has been expanding our understanding of this region. However, much is still to be learned. Understanding its functional anatomy is of utmost importance in achieving successful tumor resection. Nevertheless, further characterization in humans is needed not only to improve our understanding of functional connectivity but also to enhance treatment outcomes by tailoring personalized approaches and treatments.

Lessons

Connectomics-based assessment of brain neural networks can ease an understanding of the prognosis of neurological function after the surgical removal of tumors. The corticospinal tract and direct connectivity to the ipsilateral motor area, as well as the FAT and any other white matter tracts traveling through the corpus callosum to the contralateral SMA and pre-SMA (as a potential compensatory mechanism), need to be preserved so that patients do not experience SMA syndrome. Quantitative map analysis of functional connectivity can help reduce surgical morbidity and assist in properly evaluating patient prognosis, while providing a feasible tool for objectifying the neurosurgeon’s footprint on the patient’s brain. More studies are needed to confirm the prognostic value of connectomics and, eventually, to correlate the imaging data with more precise prognostic information—for example, reversibility, measure, and duration of any eventual postoperative deficits.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Di Ieva. Acquisition of data: Di Ieva. Analysis and interpretation of data: Di Ieva, Suero Molina. Drafting the article: Suero Molina, Di Ieva, Tait. Critically revising the article: Di Ieva, Suero Molina. Reviewed submitted version of the manuscript: Di Ieva, Suero Molina. Approved the final version of the manuscript on behalf of all authors: Di Ieva. Administrative/technical/material support: Di Ieva, Tait. Study supervision: Di Ieva.

References

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  • Collapse
  • Expand
  • FIG. 1.

    Preoperative coronal fluid-attenuated inversion recovery (FLAIR) magnetic resonance imaging (MRI) (A) and axial 18F-fluorethyl-l-tyrosine positron emission tomography (18F-FET PET)–computed tomography (B) demonstrating growth of the known remnant with no high 18F-FET uptake, suspicious for recurrence of the previously resected oligodendroglioma grade 2. Coronal diffuse tensor imaging (DTI) and resting-state functional MRI (rs-fMRI) (C) merged together on Quicktome software, potentially showing some disruption of the frontal aslant tract (FAT) (white arrow).

  • FIG. 2.

    Intraoperative neuro-navigation (Brainlab AG) showed supramaximal resection beyond the anterior (A), medial (B), posterosuperior (C), and posterolateral (D) edges of the tumor but not in its posteromedial (E) edge, which was adjacent to functional corticospinal tract, as shown on intraoperative neuromonitoring.

  • FIG. 3.

    Postoperative axial T1 FLAIR (A) and coronal T2-weighted (B) imaging demonstrating complete resection/supramaximal resection of the oligodendroglioma recurrence in all but the posterior margin, with some minor surgical changes and blood products along the medial resection cavity. There was no sign of stroke (no restrictions on diffusion-weighted imaging; not shown in the figure).

  • FIG. 4.

    Postoperative DTI and connectome imaging showing very close proximity of the surgical cavity to the sensorimotor (A), salience (B), and language (C) network parcellations, without any apparent structural and functional impairment of these networks.

  • FIG. 5.

    Pre- and postoperative quantitative anomaly matrices of the sensorimotor network of the patient compared with normative matrices generated from 200 healthy adults (A). No relevant difference could be observed between the preoperative (B) and postoperative (C) matrices of the patient, potentially confirming anatomical and functional preservation of this network (no differences were found in the other networks, including the language ones; not shown in the figure).

  • 1

    Tate MC, Kim CY, Chang EF, Polley MY, Berger MS. Assessment of morbidity following resection of cingulate gyrus gliomas. Clinical article. J Neurosurg. 2011;114(3):640647.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Baker CM, Burks JD, Briggs RG, et al. The crossed frontal aslant tract: a possible pathway involved in the recovery of supplementary motor area syndrome. Brain Behav. 2018;8(3):e00926.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Tanji J, Shima K. Supplementary motor cortex in organization of movement. Eur Neurol. 1996;36(suppl 1):1319.

  • 4

    Nachev P, Kennard C, Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci. 2008;9(11):856869.

  • 5

    Cunnington R, Windischberger C, Deecke L, Moser E. The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. Neuroimage. 2002;15(2):373385.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Omniscient Neurotechnology. Infinitome. Accessed May 27, 2023. https://o8t.com

  • 7

    Glasser MF, Coalson TS, Robinson EC, et al. A multi-modal parcellation of human cerebral cortex. Nature. 2016;536(7615):171178.

  • 8

    Sheets JR, Briggs RG, Young IM, et al. Parcellation-based modeling of the supplementary motor area. J Neurol Sci. 2021;421:117322.

  • 9

    Çavdar S, Köse B, Altınöz D, Özkan M, Güneş YC, Algın O. The brainstem connections of the supplementary motor area and its relations to the corticospinal tract: experimental rat and human 3-tesla tractography study. Neurosci Lett. 2023;798:137099.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Catani M, Mesulam MM, Jakobsen E, et al. A novel frontal pathway underlies verbal fluency in primary progressive aphasia. Brain. 2013;136(Pt 8):26192628.

  • 11

    Goulden N, Khusnulina A, Davis NJ, et al. The salience network is responsible for switching between the default mode network and the central executive network: replication from DCM. Neuroimage. 2014;99:180190.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Briggs RG, Allan PG, Poologaindran A, et al. The frontal aslant tract and supplementary motor area syndrome: moving towards a connectomic initiation axis. Cancers (Basel). 2021;13(5):1116.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Baker CM, Burks JD, Briggs RG, et al. A connectomic atlas of the human cerebrum—Chapter 4: the medial frontal lobe, anterior cingulate gyrus, and orbitofrontal cortex. Oper Neurosurg (Hagerstown). 2018;15(suppl 1):S122S174.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Briggs RG, Conner AK, Sali G, et al. A connectomic atlas of the human cerebrum—Chapter 17: tractographic description of the cingulum. Oper Neurosurg (Hagerstown). 2018;15(suppl 1):S462S469.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Poologaindran A, Lowe SR, Sughrue ME. The cortical organization of language: distilling human connectome insights for supratentorial neurosurgery. J Neurosurg. 2020;134(6):19591966.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Landers MJF, Brouwers HB, Kortman GJ, Boukrab I, De Baene W, Rutten GJM. Oligodendrogliomas tend to infiltrate the frontal aslant tract, whereas astrocytomas tend to displace it. Neuroradiology. 2023;65(7):11271131.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Ng S, Valdes PA, Moritz-Gasser S, Lemaitre AL, Duffau H, Herbet G. Intraoperative functional remapping unveils evolving patterns of cortical plasticity. Brain. 2023;146(7):30883100.

    • PubMed
    • Search Google Scholar
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