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Cited by 435Neural and Behavioral Psychology StudiesFunctional Brain Connectivity StudiesVisual perception and processing mechanisms

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Role of the anterior insula in task-level control and focal attention

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Nelson, Steven M., Dosenbach, Nico U. F., Cohen, Alexander L., Wheeler, Mark E., Schlaggar, Bradley L., Petersen, Steven E.·2010·Brain Structure and Function
DOI 10.1007/s00429-010-0260-2PMC PMC2886908
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Abstract

In humans, the anterior insula (aI) has been the topic of considerable research and ascribed a vast number of functional properties by way of neuroimaging and lesion studies. Here, we argue that the aI, at least in part, plays a role in domain-general attentional control and highlight studies (Dosenbach et al. 2006; Dosenbach et al. 2007) supporting this view. Additionally, we discuss a study (Ploran et al. 2007) that implicates aI in processes related to the capture of focal attention. Task-level control and focal attention may or may not reflect information processing supported by a single functional area (within the aI). Therefore, we apply a novel technique (Cohen et al. 2008) that utilizes resting state functional connectivity MRI (rs-fcMRI) to determine whether separable regions exist within the aI. rs-fcMRI mapping suggests that the ventral portion of the aI is distinguishable from more dorsal/anterior regions, which are themselves distinct from more posterior parts of the aI. When these regions are applied to functional MRI (fMRI) data, the ventral and dorsal/anterior regions support processes potentially related to both task-level control and focal attention, whereas the more posterior aI regions did not. These findings suggest that there exists some functional heterogeneity within aI that may subserve related but distinct types of higher-order cognitive processing.

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Fig. 1 Activation foci in bilateral anterior insula (aI) are among the most commonly found in functional neuroimaging studies. Regions of interest from 41,581 foci across 1,114 studies were used to create a foci density plot, shown here on inflated PALS atlas cortical surfaces (Caret). The map represents how often a region of interest has been reported at a particular location. Studies containing these foci were reported in the journals Neuron (2002–2008), Nature Neuroscience (2001–2008), Proceedings of the National Academy of Sciences (2006–2008), Journal of Neuroscience (1996–2008), and Cerebral Cortex (1997–2007). The locations of the foci from these studies can be accessed at http://brainvis.wustl.edu
Fig. 1 Activation foci in bilateral anterior insula (aI) are among the most commonly found in functional neuroimaging studies. Regions of interest from 41,581 foci across 1,114 studies were used to create a foci density plot, shown here on inflated PALS atlas cortical surfaces (Caret). The map represents how often a region of interest has been reported at a particular location. Studies containing these foci were reported in the journals Neuron (2002–2008), Nature Neuroscience (2001–2008), Proceedings of the National Academy of Sciences (2006–2008), Journal of Neuroscience (1996–2008), and Cerebral Cortex (1997–2007). The locations of the foci from these studies can be accessed at http://brainvis.wustl.eduCC BY-NC · PubMed Central
Fig. 2 Across a variety of tasks, bilateral anterior insula (aI) contains signals that are consistent with a general role in task-level control. The mixed blocked/event-related fMRI design allows the separate extraction of three different types of task set-related signals. Shown here is the average remaining task-related activity (left panel) after trial-related activity (right panel) has been extracted. Activity time-locked to the start of a task block (yellow) is likely important for the initiation of task sets, while activity sustained for the length of the task period (black) is likely related to the maintenance of task sets to ensure continued performance success. Error-related signals (blue) provide performance feedback on a trial-by-trial basis. Adapted from Neuron (Dosenbach et al. 2006). Copyright (2006), with permission from Elsevier
Fig. 2 Across a variety of tasks, bilateral anterior insula (aI) contains signals that are consistent with a general role in task-level control. The mixed blocked/event-related fMRI design allows the separate extraction of three different types of task set-related signals. Shown here is the average remaining task-related activity (left panel) after trial-related activity (right panel) has been extracted. Activity time-locked to the start of a task block (yellow) is likely important for the initiation of task sets, while activity sustained for the length of the task period (black) is likely related to the maintenance of task sets to ensure continued performance success. Error-related signals (blue) provide performance feedback on a trial-by-trial basis. Adapted from Neuron (Dosenbach et al. 2006). Copyright (2006), with permission from ElsevierCC BY-NC · PubMed Central
Fig. 3 The anterior insula (aI) forms part of a cingulo-opercular control network, distinct from a fronto-parietal control network. Human cingulo-opercular (black) and fronto-parietal (yellow) control networks displayed on inflated brain surfaces. The network structure of human control networks is displayed as a two-dimensional pseudo-anatomical graph layout. Black lines indicate strong resting state functional connections between brain regions. Adapted from Proceedings of the National Academy of Sciences (Dosenbach et al. 2007). Copyright (2007), with permission from National Academy of Sciences, USA
Fig. 3 The anterior insula (aI) forms part of a cingulo-opercular control network, distinct from a fronto-parietal control network. Human cingulo-opercular (black) and fronto-parietal (yellow) control networks displayed on inflated brain surfaces. The network structure of human control networks is displayed as a two-dimensional pseudo-anatomical graph layout. Black lines indicate strong resting state functional connections between brain regions. Adapted from Proceedings of the National Academy of Sciences (Dosenbach et al. 2007). Copyright (2007), with permission from National Academy of Sciences, USACC BY-NC · PubMed Central
Fig. 4 In an extended reveal paradigm, BOLD time course activity in bilateral anterior insula (aI) responds transiently at the moment of recognition. Objects were revealed from a mask of noise in 2 s steps and subjects made a button press when they could identify the object. At the end trial VoA (verification of accuracy) stage, the picture was fully revealed and subjects were asked to indicate by button press whether they had correctly identified the item as it was being revealed. Average time courses are depicted for a set of regions that showed baseline activity until subjects responded that they recognized an object being unmasked from a noise field. The activity was time-locked to the subjects’ response, resulting in a gradual shift in the onset depending upon what “step” or “reveal stage (TR4, 5, 6, 7)” the subject recognized the item. Adapted from Journal of Neuroscience (Ploran et al. 2007). Copyright (2007) with permission from the Society for Neuroscience
Fig. 4 In an extended reveal paradigm, BOLD time course activity in bilateral anterior insula (aI) responds transiently at the moment of recognition. Objects were revealed from a mask of noise in 2 s steps and subjects made a button press when they could identify the object. At the end trial VoA (verification of accuracy) stage, the picture was fully revealed and subjects were asked to indicate by button press whether they had correctly identified the item as it was being revealed. Average time courses are depicted for a set of regions that showed baseline activity until subjects responded that they recognized an object being unmasked from a noise field. The activity was time-locked to the subjects’ response, resulting in a gradual shift in the onset depending upon what “step” or “reveal stage (TR4, 5, 6, 7)” the subject recognized the item. Adapted from Journal of Neuroscience (Ploran et al. 2007). Copyright (2007) with permission from the Society for NeuroscienceCC BY-NC · PubMed Central
Fig. 5 rs-fcMRI mapping reveals locations in left anterior insula (aI) that may represent dissociable putative functional areas. a A grid of foci was placed over the extent of the left insula and surrounding cortex. 27 putative areas were defined in this “patch”, including five in the anterior-most portion of the left insula. Spheres indicating regions outside of the aI are colored in tan D (dorsal), V (ventral), A (anterior), P (posterior). b A portion of the left hemisphere surrounding the aI is enlarged to depict the five locations defined therein (black circle). Regions are separately colored and named according to their relative locations within the aI. Stereotactic coordinates are reported in MNI space
Fig. 5 rs-fcMRI mapping reveals locations in left anterior insula (aI) that may represent dissociable putative functional areas. a A grid of foci was placed over the extent of the left insula and surrounding cortex. 27 putative areas were defined in this “patch”, including five in the anterior-most portion of the left insula. Spheres indicating regions outside of the aI are colored in tan D (dorsal), V (ventral), A (anterior), P (posterior). b A portion of the left hemisphere surrounding the aI is enlarged to depict the five locations defined therein (black circle). Regions are separately colored and named according to their relative locations within the aI. Stereotactic coordinates are reported in MNI spaceCC BY-NC · PubMed Central
Fig. 6 An examination of the rs-fcMRI correlation patterns of the five putative area locations in left anterior insula (aI) reveals some distinct and overlapping patterns of functional connections. a–e rs-fcMRI correlation maps depicting regions of significant positive (dark red to yellow, z-score > 2.00) and negative (dark green to blue, z-score < −2.00) correlations with each seed are shown on left lateral and medial inflated cortical surfaces (Caret). The location of each seed is shown on the left aI view (center of figure) and also on the lateral surface of the correlation map. f The similarity between the rs-fcMRI correlation maps is quantified using eta2 and displayed as a matrix that represents the relationship between each region in the aI. Eta2 values approaching 1 are indicative of highly similar maps, whereas eta2 values near 0.5 indicate that the two maps are statistically independent from one another
Fig. 6 An examination of the rs-fcMRI correlation patterns of the five putative area locations in left anterior insula (aI) reveals some distinct and overlapping patterns of functional connections. a–e rs-fcMRI correlation maps depicting regions of significant positive (dark red to yellow, z-score > 2.00) and negative (dark green to blue, z-score < −2.00) correlations with each seed are shown on left lateral and medial inflated cortical surfaces (Caret). The location of each seed is shown on the left aI view (center of figure) and also on the lateral surface of the correlation map. f The similarity between the rs-fcMRI correlation maps is quantified using eta2 and displayed as a matrix that represents the relationship between each region in the aI. Eta2 values approaching 1 are indicative of highly similar maps, whereas eta2 values near 0.5 indicate that the two maps are statistically independent from one anotherCC BY-NC · PubMed Central
Fig. 7 Moment of recognition-like processing in anterior insula (aI). a–e For each region in aI, time courses were separately extracted for trials where the subject recognized the stimulus at each step of revelation, i.e., TR4, TR5, TR6, TR7, including only correct responses. Time courses are graphed in units of % signal change from baseline (dotted line) as a function of time in seconds
Fig. 7 Moment of recognition-like processing in anterior insula (aI). a–e For each region in aI, time courses were separately extracted for trials where the subject recognized the stimulus at each step of revelation, i.e., TR4, TR5, TR6, TR7, including only correct responses. Time courses are graphed in units of % signal change from baseline (dotted line) as a function of time in secondsCC BY-NC · PubMed Central
Fig. 8 Error processing in anterior insula (aI). a–e For each region in aI, time courses were extracted for correct responses (early = TR4 + 5 and late = TR6 + 7) and errors (early = TR4 + 5 and late = TR6 + 7). Time courses are graphed in units of % signal change from baseline (dotted line) as a function of time in seconds. A correctness × time repeated measures ANOVA was calculated for each region to identify effects of error vs correct responses. *p < 0.001
Fig. 8 Error processing in anterior insula (aI). a–e For each region in aI, time courses were extracted for correct responses (early = TR4 + 5 and late = TR6 + 7) and errors (early = TR4 + 5 and late = TR6 + 7). Time courses are graphed in units of % signal change from baseline (dotted line) as a function of time in seconds. A correctness × time repeated measures ANOVA was calculated for each region to identify effects of error vs correct responses. *p < 0.001CC BY-NC · PubMed Central

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Metadata

Authors
Nelson, S. M., Dosenbach, N. U. F., Cohen, A. L., Wheeler, M. E., Schlaggar, B. L., & Petersen, S. E.
Affiliations
  • Washington University in St. Louis (US)
  • University of Pittsburgh (US)
Corresponding author
Nelson, Steven M.
ORCID
Venue
Brain Structure and Function
Publisher
Springer Science and Business Media LLC
Published
2010-05-29
Volume
214
Issue
5-6
Pages
669-680
ISSN
  • 1863-2653 (ISSN-L)
  • 1863-2661
DOI
10.1007/s00429-010-0260-2
PMC
PMC2886908
OpenAlex
W1973254033
Cited by
435
References
65
Citations by year
2026: 11 · 2025: 12 · 2024: 15 · 2023: 20 · 2022: 28 · 2021: 23 · 2020: 26 · 2019: 25 · 2018: 34 · 2017: 31 · 2016: 37 · 2015: 41 · 2014: 31 · 2013: 48 · 2012: 28
FWCI
2.34
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Brain Structure and Function (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation
  • National Institutes of Health
  • National Institute of Neurological Disorders and Stroke (R01NS046424, K02NS053425, F30NS062489, NS46424, NS61144, NS62489, NS 41255, R21NS041255, NS53425, R21NS061144)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD057076, HD57076)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords
anterior insula, task-level control, focal attention, resting-state functional connectivity, functional heterogeneity, cognitive control, attentional capture
MeSH terms
Attention, Brain Mapping, Cerebral Cortex, Cognition, Magnetic Resonance Imaging, Nerve Net, Neural Pathways, Executive Function

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