The insula (Island of Reil) and its role in auditory processing: Literature review

doi:10.1016/S0165-0173(03)00172-3

Brain Research Reviews

Volume 42, Issue 2, May 2003, Pages 143-154

https://doi.org/10.1016/S0165-0173(03)00172-3 Get rights and content

Abstract

The insular cortex is a complex structure which contains areas that subserve visceral sensory, motor, vestibular, and somatosensory functions. The role of the insular cortex in auditory processing was poorly understood until recently. However, recent case studies indicate that bilateral damage to the insulae may result in total auditory agnosia. Functional imaging studies demonstrate that the insulae participate in several key auditory processes, such as allocating auditory attention and tuning in to novel auditory stimuli, temporal processing, phonological processing and visual–auditory integration. These studies do not clarify the issue of further specialisation within the insular cortex, e.g. whether the posterior insulae are primarily sensory areas, while the anterior insulae serve mainly as integration/association auditory areas, two hypotheses that would be compatible with the cytoarchitectonic structure and connectivity of the insulae. The functional characterisation of the insulae remains incomplete, underlining the need for further studies.

Introduction

The insula (Island of Reil—Broadman areas 13–16) is a complex structure with increased complexity in the course of primate evolution that is characterised by a striking heterogeneity in architecture, physiology and connectivity with other areas of the brain. Thus it subserves a wide range of neural processes in all species. The role of the human insular cortex as visceral sensory, motor, motor association, vestibular, and somatonsensory areas is well known [2], [3]. In contrast, its role in auditory processing is poorly understood. The aim of this review paper is to summarise and discuss the available information on the auditory functions of the human insulae.

Section snippets

Anatomy

The insula lies deep inside the lateral sulcus in the Sylvian fissure under the operculum. Removal of the fronto-orbital, frontoparietal and temporal opercula will reveal the pyramid-shaped insula in its entirety ( Fig. 1) [35]. The extreme capsule consists of the insular subcortical white matter and is united with the white matter of the opercula. The insular cortex and extreme capsule cover the claustrum, external capsule, putamen and globus pallidus (Fig. 2) [35]. The insula contains five to

Cytoarchitecture

The insular cortex is divided into three belts from anterior to posterior on the basis of a gradual cytoarchitectonic change. These include (a) an agranular belt on the anterior one-third of the insula (b) a transitional dysgranular belt in layers without complete laminar differentiation, and (c) a posterior granular belt with well defined granule cell layers that occupies the posterior third [3]. Further analysis of the cortical architecture of the human insula in cytochrome oxidase,

Connections

Regional cytoarchitectonic differences correspond well to the thalamic connectivity of the insula. Jones and Burton [21] studied the cortical connections of the thalamus in 66 rhesus and squirrel monkey brains by injecting isotopically labelled aminoacids in the thalamic nuclei complexes, including the medial geniculate body. While no axoplasmically transported label could be traced in the anterior-third agranular area, the posterior-third granular insular field had a dense, coarse thalamic

Case reports in humans

Over the last few decades, single case reports in humans have thrown some further light onto the role that the insula has in auditory processing. Subjects with vascular events that include the insulae on one or both sides may present with auditory agnosia contralaterally to the affected side, to environmental sounds [33], speech [20], music [18], or to all three of the above [15], [16], [19] and this agnosia will resolve to a varying degree over a few months to years, depending on the extent of

PET and fMRI studies

The single case studies of the previous section provide abundant support for a major role for the human insulae in auditory processing. However, the specific functional deficits that are caused by the insular lesions cannot be firmly established, due to methodology differences that include patient testing and radiology, involvement of adjacent auditory structures to a varying extent, and the patient’s own inherent characteristics pre-stroke. More sophisticated imaging techniques, such as PET or

Comments and conclusion

The insular cortex has been largely ignored as an auditory centre until recently. However, the finding of very prominent auditory deficits in patients with strokes that involved the insulae, but spared Heschl’s gyrus [16], [20], indicate that the insulae are not only an integral component of the central auditory nervous system, but vital relay stations, as its bilateral damage may result in total agnosia [19]. Sophisticated neuroimaging studies have helped to establish the insula’s specific

References (37)

J.R. Augustine
Circuitry and functional aspects of the insular lobe in primates including humans
Brain. Res. Rev.
(1996)
G.A. Calvert et al.
Detection of audio–visual integration sites in humans by application of electrophysiological criteria to the BOLD effect
NeuroImage
(2001)
J.T. Coull
Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology
Progr. Neurobiol.
(1998)
M. Habib et al.
Mutism and auditory agnosia due to bilateral insular damage-role of the insula in human communication
Neuropsychologia
(1995)
D. Pandya et al.
The topographical distribution of interhemispheric connections in the rhesus monkey
Brain Res.
(1971)
F. Rivier et al.
Cytochrome oxidase, acetylcholinesterase and NADPH-diaphorase staining in human supratemporal and insular cortex: evidence for multiple auditory areas
NeuroImage
(1997)
K. Sudakov et al.
Unit study of exteroceptive inputs to claustrocortex in awake sitting squirrel monkeys
Brain Res.
(1971)
D. Wong et al.
PET imaging of differential cortical activation by monaural speech and non-speech stimuli
Hear. Res.
(2002)
H. Ackermann et al.
Rate dependent activation of a prefrontal insular cerebellar network during passive listening to trains of click stimuli: an fMRI study
Neuroreport
(2001)
J.R. Augustine
The insular lobe in primates including humans
Neurol. Res.
(1985)

S.P. Bornstein et al.

Implications of temporal processing for children with learning and language problems

H. Burton et al.

The posterior thalamic region and its cortical projection in New World and Old World monkey

J. Comp. Neurol.

(1976)

K. Bushara et al.

Neural correlates of auditory–visual stimulus onset asynchrony detection

J. Neurosci.

(2001)

F. Clasca et al.

Insular cortex and neighboring fields in the cat: a redefinition based on cortical microarchitecture and connections with the thalamus

J. Comp. Neurol.

(1997)

F. Clasca et al.

Cortical connections of the insular and adjacent parieto-temporal fields in the cat

Cereb. Cortex

(2000)

F.B. Collavita et al.

Temporal discrimination in cats with insular–temporal lesions

Brain Res.

(1974)

D.P. Corina et al.

FMRI auditory language differences between dyslexic and able reading children

Brain Imaging

(2001)

J. Downar et al.

A cortical network sensitive to stimulus salience in a neutral behavioural context across multiple sensory modalities

J. Neurophysiol.

(2001)

Cited by (341)

Multi feature fusion network for schizophrenia classification and abnormal brain network recognition
2024, Brain Research Bulletin
Schizophrenia classification and abnormal brain network recognition have an important research significance. Researchers have proposed many classification methods based on machine learning and deep learning. However, fewer studies utilized the advantages of complementary information from multi feature to learn the best representation of schizophrenia. In this study, we proposed a multi-feature fusion network (MFFN) using functional network connectivity (FNC) and time courses (TC) to distinguish schizophrenia patients from healthy controls. DNN backbone was adopted to learn the feature map of functional network connectivity, C-RNN^AM backbone was designed to learn the feature map of time courses, and Deep SHAP was applied to obtain the most discriminative brain networks. We proved the effectiveness of this proposed model using the combining two public datasets and evaluated this model quantitatively using the evaluation indexes. The results showed that the functional network connectivity generated by independent component analysis has advantage in schizophrenia classification by comparing static and dynamic functional connections. This method obtained the best classification accuracy (ACC=87.30%, SPE=89.28%, SEN=85.71%, F1 =88.23%, and AUC=0.9081), and it demonstrated the superiority of this proposed model by comparing state-of-the-art methods. Ablation experiment also demonstrated that multi feature fusion and attention module can improve classification accuracy. The most discriminative brain networks showed that default mode network and visual network of schizophrenia patients have aberrant connections in brain networks. In conclusion, this method can identify schizophrenia effectively and visualize the abnormal brain network, and it has important clinical application value.
The neural bases of familiar music listening in healthy individuals: An activation likelihood estimation meta-analysis
2023, Neuroscience and Biobehavioral Reviews
Accumulating evidence suggests that the neural activations during music listening differs as a function of familiarity with the excerpts. However, the implicated brain areas are unclear. After an extensive literature search, we conducted an Activation Likelihood Estimation analysis on 23 neuroimaging studies (232 foci, 364 participants) to identify consistently activated brain regions when healthy adults listen to familiar music, compared to unfamiliar music or an equivalent condition. The results revealed a left cortical-subcortical co-activation pattern comprising three significant clusters localized to the supplementary motor areas (BA 6), inferior frontal gyrus (IFG, BA 44), and the claustrum/insula. Our results are discussed in a predictive coding framework, whereby temporal expectancies and familiarity may drive motor activations, despite any overt movement. Though conventionally associated with syntactic violation, our observed activation in the IFG may support a recent proposal of its involvement in a network that subserves both violation and prediction. Finally, the claustrum/insula plays an integral role in auditory processing, functioning as a hub that integrates sensory and limbic information to (sub)cortical structures.
Singing training predicts increased insula connectivity with speech and respiratory sensorimotor areas at rest
2023, Brain Research
The insula contributes to the detection of salient events during goal-directed behavior and participates in the coordination of motor, multisensory, and cognitive systems. Recent task-fMRI studies with trained singers suggest that singing experience can enhance the access to these resources. However, the long-term effects of vocal training on insula-based networks are still unknown. In this study, we employed resting-state fMRI to assess experience-dependent differences in insula co-activation patterns between conservatory-trained singers and non-singers. Results indicate enhanced bilateral anterior insula connectivity in singers relative to non-singers with constituents of the speech sensorimotor network. Specifically, with the cerebellum (lobule V-VI) and the superior parietal lobes. The reversed comparison showed no effects. The amount of accumulated singing training predicted enhanced bilateral insula co-activation with primary sensorimotor areas representing the diaphragm and the larynx/phonation area–crucial regions for cortico-motor control of complex vocalizations—as well as the bilateral thalamus and the left putamen. Together, these findings highlight the neuroplastic effect of expert singing training on insula-based networks, as evidenced by the association between enhanced insula co-activation profiles in singers and the brain's speech motor system components.
Localizing and lateralizing value of auditory phenomena in seizures
2023, Epilepsy and Behavior
Auditory seizures (AS) are a rare type of focal seizures. AS are classically thought to involve a seizure onset zone (SOZ) in the temporal lobe, but there remain uncertainties about their localizing and lateralizing value. We conducted a narrative literature review with the aim of providing an up-to-date description of the lateralizing and localizing value of AS.
The databases PubMed, Scopus, and Google Scholar were searched for literature on AS in December 2022. All cortical stimulation studies, case reports, and case series were analyzed to assess for auditory phenomena that were suggestive of AS and to evaluate if the lateralization and/or localization of the SOZ could be determined. We classified AS according to their semiology (e.g., simple hallucination versus complex hallucination) and the level of evidence with which the SOZ could be predicted.
A total of 174 cases comprising 200 AS were analyzed from 70 articles. Across all studies, the SOZ of AS were more often in the left (62%) than in the right (38%) hemisphere. AS heard bilaterally followed this trend. Unilaterally heard AS were more often due to a SOZ in the contralateral hemisphere (74%), although they could also be ipsilateral (26%). The SOZ for AS was not limited to the auditory cortex, nor to the temporal lobe. The areas more frequently involved in the temporal lobe were the superior temporal gyrus (STG) and mesiotemporal structures. Extratemporal locations included parietal, frontal, insular, and rarely occipital structures.
Our review highlighted the complexity of AS and their importance in the identification of the SOZ. Due to the limited data and heterogeneous presentation of AS in the literature, the patterns associated with different AS semiologies warrant further research.
Neural correlates of perceived emotions in human insula and amygdala for auditory emotion recognition
2022, NeuroImage
The emotional status of a speaker is an important non-linguistic cue carried by human voice and can be perceived by a listener in vocal communication. Understanding the neural circuits involved in processing emotions carried by human voice is crucial for understanding the neural basis of social interaction. Previous studies have shown that human insula and amygdala responded more selectively to emotional sounds than non-emotional sounds. However, it is not clear whether the neural selectivity to emotional sounds in these brain structures is determined by the emotion presented by a speaker which is associated with the acoustic properties of the sounds or by the emotion perceived by a listener. In this study, we recorded intracranial electroencephalography (iEEG) responses to emotional human voices while subjects performed emotion recognition tasks. We found that the iEEG responses of Heschl's gyrus (HG) and posterior insula were determined by the presented emotion, whereas the iEEG responses of anterior insula and amygdala were driven by the perceived emotion. These results suggest that the anterior insula and amygdala play a crucial role in conscious perception of emotions carried by human voice.
Cytoarchitecture, probability maps and segregation of the human insula
2022, NeuroImage
The human insular cortex supports multifunctional integration including interoceptive, sensorimotor, cognitive and social-emotional processing. Different concepts of the underlying microstructure have been proposed over more than a century. However, a 3D map of the cytoarchitectonic segregation of the insula in standard reference space, that could be directly linked to neuroimaging experiments addressing different cognitive tasks, is not yet available. Here we analyzed the middle posterior and dorsal anterior insula with image analysis and a statistical mapping procedure to delineate cytoarchitectonic areas in ten human postmortem brains. 3D-probability maps of seven new areas with granular (Ig3, posterior), agranular (Ia1, posterior) and dysgranular (Id2-Id6, middle to dorsal anterior) cytoarchitecture have been calculated to represent the new areas in stereotaxic space. A hierarchical cluster analysis based on cytoarchitecture resulted in three distinct clusters in the superior posterior, inferior posterior and dorsal anterior insula, providing deeper insights into the structural organization of the insula. The maps are openly available to support future studies addressing relations between structure and function in the human insula.

View all citing articles on Scopus

View full text

ReviewThe insula (Island of Reil) and its role in auditory processing: Literature review

Abstract

Introduction

Section snippets

Anatomy

Cytoarchitecture

Connections

Case reports in humans

PET and fMRI studies

Comments and conclusion

Brain. Res. Rev.

NeuroImage

Progr. Neurobiol.

Neuropsychologia

Brain Res.

NeuroImage

Brain Res.

Hear. Res.

Rate dependent activation of a prefrontal insular cerebellar network during passive listening to trains of click stimuli: an fMRI study

Neuroreport

The insular lobe in primates including humans

Neurol. Res.

Implications of temporal processing for children with learning and language problems

The posterior thalamic region and its cortical projection in New World and Old World monkey

J. Comp. Neurol.

Neural correlates of auditory–visual stimulus onset asynchrony detection

J. Neurosci.

Insular cortex and neighboring fields in the cat: a redefinition based on cortical microarchitecture and connections with the thalamus

J. Comp. Neurol.

Cortical connections of the insular and adjacent parieto-temporal fields in the cat

Cereb. Cortex

Temporal discrimination in cats with insular–temporal lesions

Brain Res.

FMRI auditory language differences between dyslexic and able reading children

Brain Imaging

A cortical network sensitive to stimulus salience in a neutral behavioural context across multiple sensory modalities

J. Neurophysiol.

Review
The insula (Island of Reil) and its role in auditory processing: Literature review