Functional mapping and effective connectivity of the human operculum

• Published in: Cortex Vol. 109; pp. 303 - 321
• Main Authors: Mălîia, Mihai-Dragoş, Donos, Cristian, Barborica, Andrei, Popa, Irina, Ciurea, Jean, Cinatti, Sandra, Mîndruţă, Ioana
• Format: Journal Article
• Language: English
• Published: Italy Elsevier Ltd 01.12.2018
• Subjects: Brain stimulation; Effective connectivity; Functional mapping; Operculum; Stereoelectroencephalography; MTG; Q3; IPL; DMPFC; STG; aI; Functional mapping; Operculum; SPL; CCEP; Th; VMPFC; Stereoelectroencephalography; DNET; Hc; V1; AC; AD; FCD; SMA; MT; PrCO; CEN; preSMA; fMRI; PCC; SII; PCL; Effective connectivity; SEP; A; C; PIVC; BG; E; MRI; F; ProM; VLPFC; PHG; O; R; SEEG; TPO; rsfMRI; S; OF; pI; SN; PrC; ACC; DLPFC; DMN; OpF; PMC; Brain stimulation; MCC; SPES; OpP; NRESP; OpR; CT; OpT; DES; PC; RMS; LG; MOFC; TP; ITG; LI
• ISSN: 0010-9452; 1973-8102
• DOI: 10.1016/j.cortex.2018.08.024

The operculum, defined as the cortex adjacent to the insula, is a large structure encompassing three lobes, with a recognized role in a variety of neurologic and psychiatric conditions. Its complex functions include sensory, motor, autonomic and cognitive processing. In humans, these are extended with the addition of language. These functions are implemented by highly specialized neuronal populations and their widespread connections, which our study aims at mapping in detail. We studied a group of 31 patients that were explored with intracranial electrodes during the pre-surgical workup for drug-resistant epilepsy. We have selected the subset of contacts implanted in non-epileptogenic opercular cortex and we analyzed the neurophysiological and behavioral responses to direct electrical stimulation. The functional mapping was performed by applying 1 Hz and 50 Hz electrical stimulation on 252 contact pairs and recording the threshold for evoking clinical effects. The effective connectivity was assessed using cortico-cortical evoked potentials elicited by single-pulse electrical stimulation in a subset of 19 patients. The locations of the effects grouped in twelve distinct semiological classes were analyzed. The most frequent effects evoked by stimulation of the frontal operculum were language related (29%). The Rolandic area produced most often oropharyngeal symptoms (47%), the parietal operculum produced somatosensory effects (67%), while the temporal evoked auditory (58%) semiology. The connectivity pattern was complex, with these structures having widespread ipsilateral and contralateral projections. The local connections between the opercular subregions and with the insula, as well as with more distant areas like the cingulate gyrus, were distinguished by strength and between-subjects consistency. In conclusion, we demonstrate specific opercular functionality, distinct from the one of the insular cortex. The study is complemented by a literature review on the opercular functional connectome in human and non-human primates.