Localized Preferences of Gliomas within the Action Circuit
Poster No:
1166
Submission Type:
Abstract Submission
Authors:
Jiayi Zhu1,2, Weigang Cui1, Zeya Yan3,4, Jianxun Ren1, Zhenyu Sun1, Xiaoxuan Fu1, Yinyan Wang5, Hesheng Liu1,6
Institutions:
1Changping Laboratory, Beijing, China, 2State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China, 3Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China, 4Beijing Neurosurgical Institute, Capital Medical University, Beijing, China, 5Beijing Tiantan Hospital, Capital Medical University, Beijing, China, 6Biomedical Pioneering Innovation Center, Peking University, Beijing, China
First Author:
Jiayi Zhu
Changping Laboratory|State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University
Beijing, China|Beijing, China
Changping Laboratory|State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University
Beijing, China|Beijing, China
Co-Author(s):
Zeya Yan
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University|Beijing Neurosurgical Institute, Capital Medical University
Beijing, China|Beijing, China
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University|Beijing Neurosurgical Institute, Capital Medical University
Beijing, China|Beijing, China
Hesheng Liu
Changping Laboratory|Biomedical Pioneering Innovation Center, Peking University
Beijing, China|Beijing, China
Changping Laboratory|Biomedical Pioneering Innovation Center, Peking University
Beijing, China|Beijing, China
Introduction:
Gliomas, the most common brain tumors, exhibit infiltrative growth and heterogeneous localization patterns (Weller, 2015), preferentially affecting regions like the insula, temporal cortex, and putamen (Numan, 2022). While traditional explanations have focused on structural factors like white matter pathways and vascular supply, emerging evidence points to the role of functional connectivity in glioma progression (Venkatesh, 2019). Studies using electrocorticography and task-evoked functional magnetic resonance imaging (fMRI) suggest that gliomas interact with neural circuits, potentially driving tumor growth through neuron-glioma communication (Krishna, 2023; Cui, 2022). Task-evoked neuronal hyperactivity, observed prominently in these circuits, may influence glioma growth and spatial distribution (Numan, 2022; Krishna, 2023). This suggests that gliomas preferentially localize within functionally connected networks rather than isolated regions.
Given the prominence of task-evoked neuronal activity in action-related regions, we hypothesized that gliomas preferentially localize within an action-related functional circuit.
Given the prominence of task-evoked neuronal activity in action-related regions, we hypothesized that gliomas preferentially localize within an action-related functional circuit.
Methods:
This study included a total of 1,445 glioma patients from five independent neuroimaging datasets. By leveraging resting-state functional connectomes, we developed a novel 'tumor network mapping' (TNM) approach, adapted from lesion network mapping (Stubbs, 2023), to identify the functional connectivity patterns associated with gliomas. We then examined whether these functional maps overlapped significantly with action-related functional networks across the cerebral cortex (Yeo, 2011; Dosenbach, 2024), subcortex (Tian, 2020) and cerebellum (King, 2019). To assess the generalizability of the TNM map, we validated it on two glioma spatial subtypes: cerebellar glioma and multifocal glioma datasets.
To explore the relationship between the TNM map and cognitive-behavioral processes, we leveraged the NeuroSynth database, incorporating 1,334 term-based whole-brain activation maps. Finally, we assessed the functional properties of the glioma network by correlating these patterns with the distributions of 18 neurotransmitter receptors and transporters from the Neuromap toolbox.
To explore the relationship between the TNM map and cognitive-behavioral processes, we leveraged the NeuroSynth database, incorporating 1,334 term-based whole-brain activation maps. Finally, we assessed the functional properties of the glioma network by correlating these patterns with the distributions of 18 neurotransmitter receptors and transporters from the Neuromap toolbox.
Results:
As hypothesized, gliomas exhibit a spatially heterogeneous but functionally coherent distribution across the brain (Fig. 1a, 1b). These gliomas can be organized into a replicable functional network spanning the cerebral cortex (Fig. 1c, 1d), subcortex, and cerebellum, converging on a specific functional circuit, i.e., the action circuit. Specifically, the glioma network showed significant overlap with cerebral regions associated with the action mode network and somatomotor network (Fig. 1e), as well as subcortical nuclei, including the posterior putamen, posterior globus pallidus, and ventroposterior thalamus. In the cerebellum, action-related lobes IV–VI and VIIIA/B were also prominent. For both glioma spatial subtypes, tumors primarily localized within the positive regions of the TNM map, demonstrating the generalizability of this functional network across gliomas with varying spatial subtypes.
Meta-analytic network annotation revealed that these regions are predominantly linked to action initiation, execution and feedback (Fig. 2a, 2b). Moreover, neurotransmitter receptors and transporters associated with acetylcholine, dopamine, and serotonin, which are essential for goal-directed actions, were found to be more densely distributed within the glioma network (Fig. 2c).
Meta-analytic network annotation revealed that these regions are predominantly linked to action initiation, execution and feedback (Fig. 2a, 2b). Moreover, neurotransmitter receptors and transporters associated with acetylcholine, dopamine, and serotonin, which are essential for goal-directed actions, were found to be more densely distributed within the glioma network (Fig. 2c).
·Fig. 1 | Glioma Network Overlap with Action-Related Circuits.
·Fig. 2 | Cognitive functions and neurochemical properties of the TNM map.
Conclusions:
In summary, our findings validate the hypothesis regarding the preferential localization of gliomas within the functional circuit associated with action. This research enhances our understanding of glioma distribution based on the lens of functional connectivity patterns and further substantiates the role of action-related circuit in glioma development.
Modeling and Analysis Methods:
Connectivity (eg. functional, effective, structural) 1
fMRI Connectivity and Network Modeling 2
Neuroanatomy, Physiology, Metabolism and Neurotransmission:
Anatomy and Functional Systems
Keywords:
Cerebellum
Cortex
Data analysis
FUNCTIONAL MRI
Modeling
MRI
STRUCTURAL MRI
Sub-Cortical
Other - glioma
1|2Indicates the priority used for review
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Provide references using APA citation style.
Dosenbach, N. U. (2024). The brain’s cingulo-opercular action-mode network. Preprint at PsyArXiv https://doi. org/10.31234/osf. io/2vt79.
King, M. (2019). Functional boundaries in the human cerebellum revealed by a multi-domain task battery. Nature neuroscience, 22(8), 1371-1378.
Krishna, S. (2023). Glioblastoma remodelling of human neural circuits decreases survival. Nature, 617(7961), 599-607.
Numan, T. (2022). Regional healthy brain activity, glioma occurrence and symptomatology. Brain, 145(10), 3654-3665.
Stubbs, J. L. (2023). Heterogeneous neuroimaging findings across substance use disorders localize to a common brain network. Nature Mental Health, 1(10), 772-781.
Tian, Y. (2020). Topographic organization of the human subcortex unveiled with functional connectivity gradients. Nature neuroscience, 23(11), 1421-1432.
Venkatesh, H. (2019). Electrical and synaptic integration of glioma into neural circuits. Nature, 573(7775), 539-545.
Weller, M. (2015). Glioma. Nature reviews Disease primers, 1(1), 1-18.
Yeo, B. T. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of neurophysiology.