Differential Role Of Insular Subdivisions In Sensory Information Processing

Insula is a region located under the lateral fissure of human brain,which is an essential area for both interoception and exteroception.It is also known to play an important role in detecting and processing deviant(novel)information.While its involvement in representation of multiple dimensions of sensory information has been well characterized,there is still a lack of understanding how insula processes deviant information.This study sought to examine how physical parameters(e.g.,audio frequency)and deviance of auditory stimulation were processed in sub-regions of insula,using the high spatiotemporal resolution stereo-electroencephalography(sEEG).A total of 15 epileptic patients(male 10,female 5)with surgically implanted electrodes were included in the study.We used a classical Oddball paradigm which includes standard and deviant auditory stimulations with high(1500 Hz)or low(800 Hz)audio frequency.Intracranial EEG signals were recorded simultaneously.Data were collected from 118 recording sites located within the right insula(posterior 57,anterior 61).The analysis of event-related potentials(ERPs)indicated that a negative wave N1 with a latency of ~128 ms was evoked by either standard or deviant auditory stimulation.In addition,a later positive wave P3 with a latency of ~285 ms was exclusively evoked by the deviant stimulation.Regression analysis of MNI coordinates and ERPs revealed that the ERP tended to change along the direction of the Y-axis with 45 degree clockwise rotation.Thus,along the direction from the dorsal posterior side to the ventral anterior side of the insula,the changes included decrease in N1,prolongation of latencies of both N1 and P3 and the increase in P3 amplitude.By further analyzing each of subareas of the insula,however,we found that significant change of N1 and P3 amplitudes only reserved in subdivisions of the posterior(PI)and anterior insula(AI),respectively.In addition,the N1 amplitude was responsive to the audio frequencies of standard stimulation.Both the amplitude and latency of N1 evoked by deviant stimulations were significantly greater than that evoked by standard stimulation.A further decoding analysis showed that the posterior insula identified the frequency feature of the auditory stimulation at an earlier time point,while the anterior insula was able to detect the deviance with a longer time window.For a better understanding of the role of insula in sensory processing and cognitive function,the time-frequency analysis was performed on sound evoked activity in the insula.We found that,compared with the standard stimulation,the deviant stimulation caused a significantly greater increase in the powers of ?(4-8 Hz),?(9-14 Hz),and high-?(105-120 Hz)oscillations.It seems that,while high-? was involved in detecting the frequency feature of both standard and deviant stimulations,the ?,? and mid-?(60-90 Hz)oscillations only reflected that of deviant stimulation.In addition,the activation of ? oscillation was greater in posterior than anterior insula.Our results suggest that N1,mid-? and high-? oscillations likely reflected physical properties of stimulation,while P3,? and ? oscillations represented the processing of deviance in insula.Auditory signals probably reached the dorsal posterior part of insula first,and then travelled to the ventral anterior part and was processed continuously along this direction.The dorsal posterior PI tended to process physical property of sound while the ventral anterior AI tented to process deviance detection.Furthermore,during the auditory signal processing,the communication between the anterior and posterior insula was achieved by modulating each other's high frequency neural activity with own ? and ? oscillations.In conclusion,our study demonstrated that dorsal posterior part of the posterior insula was the core region for processing physical property of sensory stimulation,while ventral anterior part of the anterior insula was the core region for detecting deviance.The communication between AI and PI was achieved through ? and ? band oscillations.