A vertigo network derived from human brain lesions and brain stimulation

Author:

Li Yanran1ORCID,Qi Lei1ORCID,Schaper Frédéric L W V J234,Wu Di1,Friedrich Maximilian2345ORCID,Du Jialin16,Yu Tao7,Wang Qiao1,Wang Xiaopeng1,Wang Di8,Jin Guangyuan1,Liu Aihua1,Fan Chunqiu1,Wang Yuping1,Fox Michael D2349,Ren Liankun110ORCID

Affiliation:

1. Department of Neurology, Clinical Center for Epilepsy, Xuanwu Hospital, Capital Medical University, National Center for Neurological Disorders , Beijing 100053 , China

2. Center for Brain Circuit Therapeutics, Department of Neurology, Brigham and Women’s Hospital, Harvard Medical School , Boston, MA 02115 , USA

3. Department of Psychiatry, Brigham and Women’s Hospital, Harvard Medical School , Boston, MA 02115 , USA

4. Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School , Boston, MA 02115 , USA

5. Department of Neurology, University Hospital Wuerzburg , Josef-Schneider Strasse 11, Wuerzburg 97080 , Germany

6. Department of Pharmacy Phase I Clinical Trial Center, Xuanwu Hospital, Capital Medical University , Beijing 100053 , China

7. Department of Functional Neurosurgery, Beijing Institute of Functional Neurosurgery, Xuanwu Hospital, Clinical Center for Epilepsy, Capital Medical University , Beijing 100053 , China

8. School of Engineering Medicine, Beihang University , Beijing 100191 , China

9. Athinoula A. Martino’s Center for Biomedical Imaging, Departments of Neurology and Radiology, Massachusetts General Hospital , Boston, MA 02114 , USA

10. Chinese Institute for Brain Research , Beijing 102206 , China

Abstract

AbstractVertigo is a common neurological complaint, which can result in significant morbidity and decreased quality of life. While pathology to peripheral and subtentorial brain structures is a well-established cause of vertigo, cortical lesions have also been linked to vertigo and may lend insight into relevant neuroanatomy. Here, we investigate the supratentorial lesion locations associated with vertigo and test whether they map to a common brain network. We performed a systematic literature search and identified 23 cases of supratentorial brain lesions associated with vertigo. We mapped the lesion locations to a standard brain template and computed the network of brain regions functionally connected to each lesion location, using a ‘wiring diagram’ of the human brain termed the human connectome (n = 1000). Sensitivity was assessed by identifying the most common connection to lesion locations associated with vertigo, and specificity was assessed through comparison with control lesions associated with symptoms other than vertigo (n = 68). We found that functional connectivity between lesion locations and the bilateral ventral posterior insula was both sensitive (22/23 lesions) and specific (voxel-wise family-wise error-corrected P < 0.05) for lesion-induced vertigo. We computed connectivity with this hub region to define a lesion-based vertigo network, which included regions in the bilateral insula, somatosensory cortex, higher-level visual areas, cingulate sulcus, thalamus and multiple cerebellar regions in the territory of the posterior inferior cerebellar artery. Next, we used stereo-electroencephalography (80 stimulation sites across 17 patients) to test whether stimulation sites associated with vertigo mapped to this same network. We found that 36/42 (86%) of stimulation sites eliciting vertigo fell within the lesion-based vertigo network in contrast to 16/39 (41%) of stimulation sites that did not elicit vertigo. Connectivity between stimulation sites and our lesion-based hub in the ventral posterior insula was also significantly associated with vertigo (P < 0.0001). We conclude that cortical lesions and direct electrical stimulation sites associated with vertigo map to a common brain network, offering insights into the causal neuroanatomical substrate of vertigo.

Funder

Natural Science Foundation of Beijing Municipality

National Natural Science Foundation of China

Cooperation Project of Chinese Institute for Brain Research, Beijing

Beijing Municipal Science and Technology Commission

National Key Research and Development Program of China

Publisher

Oxford University Press (OUP)

Subject

Neurology,Cellular and Molecular Neuroscience,Biological Psychiatry,Psychiatry and Mental health

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