Subjective states induced by intracranial electrical stimulation matches the cytoarchitectonic organization of the human insula

Direct electrical stimulation of the human insular cortex in 17 neurosurgical patients with 142 implanted electrodes induced reportable changes in conscious experience at 40% of stimulation sites, spanning visceral/autonomic, anxiety, taste/olfactory, pain/temperature, and somatosensory domains. These subjective responses mapped onto specific microstructural areas defined by cytoarchitectonic parcellation: pain and thermal responses localized to areas lg2/ld2, non-painful somatosensory responses to area ld3, and visceroceptive responses to area Id6. Stimulation of area Id7 in the dorsal anterior insula did not produce reportable subjective changes, despite intracranial EEG recordings showing significant time-locked high-frequency activity. The findings provide a multimodal functional map linking fine-grained microstructural subdivisions to distinct subjective experiences.

Study at a glance

Abstract

Functions of the human insula have been explored extensively with neuroimaging methods and intracranial electrical stimulation studies that have highlighted a functional segregation across its subregions. A recently developed cytoarchitectonic map of the human insula has also segregated this brain region into various areas. Our knowledge of the functional organization of this brain region at the level of these fine-parceled microstructural areas remains only partially understood. We address this gap of knowledge by applying a multimodal approach linking direct electrical stimulation and task-evoked intracranial EEG recordings with microstructural subdivisions of the human insular cortex. In 17 neurosurgical patients with 142 implanted electrodes, stimulation of 40 % of the sites induced a reportable change in the conscious experience of the subjects in visceral/autonomic, anxiety, taste/olfactory, pain/temperature as well as somatosensory domains. These subjective responses showed a topographical allocation to microstructural areas defined by probabilistic cytoarchitectonic parcellation maps of the human insula. We found the pain and thermal responses to be located in areas lg2/ld2, while non-painful/non-thermal somatosensory responses corresponded to area ld3 and visceroceptive responses to area Id6. Lastly, the stimulation of area Id7 in the dorsal anterior insula, failed to induce reportable changes to subjective experience even though intracranial EEG recordings from this region captured significant time-locked high-frequency activity (HFA). Our results provide a multimodal map of functional subdivisions within the human insular cortex at the individual brain basis and characterize their anatomical association with fine-grained cytoarchitectonic parcellations of this brain structure.