Role of the anterior insular cortex in integrative causal signaling during multisensory auditory-visual attention

European Journal of Neuroscience

Volumn 41, Issue 2, 2015, Pages 264-274

  Chen, Tianwen ^a   Michels, Lars ^a,b   Supekar, Kaustubh ^a   Kochalka, John ^a   Ryali, Srikanth ^a   Menon, Vinod ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Anterior insular cortex; Central executive network; Multisensory attention; Multivariate dynamical system model; Oddball; Salience network

Indexed keywords

ADULT; ANTERIOR INSULAR CORTEX; ARTICLE; ATTENTION; AUDITORY ATTENTION; AUDITORY STIMULATION; BEHAVIOR; BOLD SIGNAL; BRAIN FUNCTION; BRAIN REGION; CENTRAL EXECUTIVE NETWORK; CINGULATE GYRUS; COGNITION; CONTROLLED STUDY; DORSAL ANTERIOR CINGULATE CORTEX; DYNAMICS; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NERVE CELL NETWORK; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL CORTEX; POSTERIOR PARIETAL CORTEX; PREFRONTAL CORTEX; RIGHT HEMISPHERE; SALIENCE NETWORK; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SUPERIOR TEMPORAL SULCUS; TASK PERFORMANCE; VISUAL ATTENTION; VISUAL STIMULATION; ADOLESCENT; BIOLOGICAL MODEL; BRAIN CORTEX; BRAIN MAPPING; HEARING; NEUROPSYCHOLOGICAL TEST; PHOTOSTIMULATION; PHYSIOLOGY; VISION; YOUNG ADULT;

ACOUSTIC STIMULATION; ADOLESCENT; ADULT; ATTENTION; AUDITORY PERCEPTION; BRAIN MAPPING; CEREBRAL CORTEX; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; NEUROPSYCHOLOGICAL TESTS; PHOTIC STIMULATION; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84921025139     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12764     Document Type: Article

References (55)

1. Anderson, J.S., Ferguson, M.A., Lopez-Larson, M. & Yurgelun-Todd, D. (2010) Topographic maps of multisensory attention. Proc. Natl. Acad. Sci. USA, 107, 20110-20114.
2. Augustine, J.R. (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Rev., 22, 229-244.
3. Bamiou, D.E., Musiek, F.E. & Luxon, L.M. (2003) The insula (Island of Reil) and its role in auditory processing. Literature review. Brain Res. Brain Res. Rev., 42, 143-154.
4. Baum, S.H., Martin, R.C., Hamilton, A.C. & Beauchamp, M.S. (2012) Multisensory speech perception without the left superior temporal sulcus. NeuroImage, 62, 1825-1832.
5. Beckmann, C.F., DeLuca, M., Devlin, J.T. & Smith, S.M. (2005) Investigations into resting-state connectivity using independent component analysis. Philos. T. Roy. Soc. B., 360, 1001-1013.
6. Bushara, K.O., Grafman, J. & Hallett, M. (2001) Neural correlates of auditory-visual stimulus onset asynchrony detection. J. Neurosci., 21, 300-304.
7. Bushara, K.O., Hanakawa, T., Immisch, I., Toma, K., Kansaku, K. & Hallett, M. (2003) Neural correlates of cross-modal binding. Nat. Neurosci., 6, 190-195.
8. Butti, C. & Hof, P.R. (2010) The insular cortex: a comparative perspective. Brain Struct. Funct., 214, 477-493.
9. Calvert, G.A., Campbell, R. & Brammer, M.J. (2000) Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex. Curr. Biol., 10, 649-657.
10. Calvert, G.A., Hansen, P.C., Iversen, S.D. & Brammer, M.J. (2001) Detection of audio-visual integration sites in humans by application of electrophysiological criteria to the BOLD effect. NeuroImage, 14, 427-438.
11. Cappe, C., Thut, G., Romei, V. & Murray, M.M. (2010) Auditory-visual multisensory interactions in humans: timing, topography, directionality, and sources. J. Neurosci., 30, 12572-12580.
12. Cho, S., Metcalfe, A.W., Young, C.B., Ryali, S., Geary, D.C. & Menon, V. (2012) Hippocampal-prefrontal engagement and dynamic causal interactions in the maturation of children's fact retrieval. J. Cognitive Neurosci., 24, 1849-1866.
13. Corbetta, M. & Shulman, G.L. (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci., 3, 201-215.
14. Crottaz-Herbette, S. & Menon, V. (2006) Where and when the anterior cingulate cortex modulates attentional response: combined fMRI and ERP evidence. J. Cognitive Neurosci., 18, 766-780.
15. Debener, S., Kranczioch, C., Herrmann, C.S. & Engel, A.K. (2002) Auditory novelty oddball allows reliable distinction of top-down and bottom-up processes of attention. Int. J. Psychophysiol., 46, 77-84.
16. Debener, S., Makeig, S., Delorme, A. & Engel, A.K. (2005) What is novel in the novelty oddball paradigm? Functional significance of the novelty P3 event-related potential as revealed by independent component analysis. Brain Res. Cogn. Brain Res., 22, 309-321.
17. Dosenbach, N.U., Fair, D.A., Miezin, F.M., Cohen, A.L., Wenger, K.K., Dosenbach, R.A., Fox, M.D., Snyder, A.Z., Vincent, J.L., Raichle, M.E., Schlaggar, B.L. & Petersen, S.E. (2007) Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. USA, 104, 11073-11078.
18. Dosenbach, N.U., Fair, D.A., Cohen, A.L., Schlaggar, B.L. & Petersen, S.E. (2008) A dual-networks architecture of top-down control. Trends Cogn. Sci., 12, 99-105.
19. Driver, J. & Noesselt, T. (2008) Multisensory interplay reveals crossmodal influences on 'sensory-specific' brain regions, neural responses, and judgments. Neuron, 57, 11-23.
20. Eckert, M.A., Menon, V., Walczak, A., Ahlstrom, J., Denslow, S., Horwitz, A. & Dubno, J.R. (2009) At the heart of the ventral attention system: the right anterior insula. Hum. Brain Mapp., 30, 2530-2541.
21. Friston, K.J., Holmes, A.P., Poline, J.B., Grasby, P.J., Williams, S.C., Frackowiak, R.S. & Turner, R. (1995) Analysis of fMRI time-series revisited. NeuroImage, 2, 45-53.
22. Glover, G.H. & Lai, S. (1998) Self-navigated spiral fMRI: interleaved versus single-shot. Magn. Reson. Med., 39, 361-368.
23. Glover, G.H. & Law, C.S. (2001) Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn. Reson. Med., 46, 515-522.
24. Gogolla, N., Takesian, A.E., Feng, G., Fagiolini, M. & Hensch, T.K. (2014) Sensory integration in mouse insular cortex reflects GABA circuit maturation. Neuron, 83, 894-905.
25. Kiehl, K.A. & Liddle, P.F. (2003) Reproducibility of the hemodynamic response to auditory oddball stimuli: a six-week test-retest study. Hum. Brain Mapp., 18, 42-52.
26. Linden, D.E., Prvulovic, D., Formisano, E., Vollinger, M., Zanella, F.E., Goebel, R. & Dierks, T. (1999) The functional neuroanatomy of target detection: an fMRI study of visual and auditory oddball tasks. Cereb. Cortex, 9, 815-823.
27. Macaluso, E., George, N., Dolan, R., Spence, C. & Driver, J. (2004) Spatial and temporal factors during processing of audiovisual speech: a PET study. NeuroImage, 21, 725-732.
28. Menon, V. & Uddin, L.Q. (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct., 214, 655-667.
29. Mesulam, M.M. & Mufson, E.J. (1982) Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. J. Comp. Neurol., 212, 1-22.
30. Molholm, S. & Foxe, J.J. (2010) Making sense of multisensory integration. Eur. J. Neurosci., 31, 1709-1712.
31. Molholm, S., Sehatpour, P., Mehta, A.D., Shpaner, M., Gomez-Ramirez, M., Ortigue, S., Dyke, J.P., Schwartz, T.H. & Foxe, J.J. (2006) Audio-visual multisensory integration in superior parietal lobule revealed by human intracranial recordings. J. Neurophysiol., 96, 721-729.
32. Mufson, E.J., Mesulam, M.M. & Pandya, D.N. (1981) Insular interconnections with the amygdala in the rhesus monkey. Neuroscience, 6, 1231-1248.
33. Nichols, T. & Hayasaka, S. (2003) Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat. Methods Med. Res., 12, 419-446.
34. Nieuwenhuys, R. (2012) The insular cortex. A review. Prog. Brain Res., 195, 123-163.
35. Nimchinsky, E.A., Gilissen, E., Allman, J.M., Perl, D.P., Erwin, J.M. & Hof, P.R. (1999) A neuronal morphologic type unique to humans and great apes. Proc. Natl. Acad. Sci. USA, 96, 5268-5273.
36. Noesselt, T., Rieger, J.W., Schoenfeld, M.A., Kanowski, M., Hinrichs, H., Heinze, H.J. & Driver, J. (2007) Audiovisual temporal correspondence modulates human multisensory superior temporal sulcus plus primary sensory cortices. J. Neurosci., 27, 11431-11441.
37. Noesselt, T., Bergmann, D., Heinze, H.J., Munte, T. & Spence, C. (2012) Coding of multisensory temporal patterns in human superior temporal sulcus. Front. Integr. Neurosci., 6, 64.
38. Oldfield, R.C. (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97-113.
39. Otto, T.U., Dassy, B. & Mamassian, P. (2013) Principles of multisensory behavior. J. Neurosci., 33, 7463-7474.
40. Roebroeck, A., Formisano, E. & Goebel, R. (2005) Mapping directed influence over the brain using Granger causality and fMRI. NeuroImage, 25, 230-242.
41. Romanski, L.M. (2007) Representation and integration of auditory and visual stimuli in the primate ventral lateral prefrontal cortex. Cereb. Cortex, 17(Suppl 1), i61-i69.
42. Romanski, L.M. (2012a) Frontiers in Neuroscience: Convergence of Auditory, Visual, and Somatosensory Information in Ventral Prefrontal Cortex. In Murray, M.M. & Wallace, M.T. (Eds), The Neural Bases of Multisensory Processes. CRC Press LLC, Boca Raton (FL).
43. Romanski, L.M. (2012b) Integration of faces and vocalizations in ventral prefrontal cortex: implications for the evolution of audiovisual speech. Proc. Natl. Acad. Sci. USA, 109(Suppl 1), 10717-10724.
44. Ryali, S., Supekar, K., Chen, T. & Menon, V. (2011) Multivariate dynamical systems models for estimating causal interactions in fMRI. NeuroImage, 54, 807-823.
45. Seeley, W.W., Menon, V., Schatzberg, A.F., Keller, J., Glover, G.H., Kenna, H., Reiss, A.L. & Greicius, M.D. (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci., 27, 2349-2356.
46. Seth, A.K. (2010) A MATLAB toolbox for Granger causal connectivity analysis. J. Neurosci. Meth., 186, 262-273.
47. Sinnett, S., Soto-Faraco, S. & Spence, C. (2008) The co-occurrence of multisensory competition and facilitation. Acta Psychol., 128, 153-161.
48. Spence, C. (2009) Explaining the Colavita visual dominance effect. Prog. Brain Res., 176, 245-258.
49. Sridharan, D., Levitin, D.J. & Menon, V. (2008) A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc. Natl. Acad. Sci. USA, 105, 12569-12574.
50. Sterzer, P. & Kleinschmidt, A. (2010) Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct. Funct., 214, 611-622.
51. Supekar, K. & Menon, V. (2012) Developmental maturation of dynamic causal control signals in higher-order cognition: a neurocognitive network model. PLoS Comput. Biol., 8, e1002374.
52. Talsma, D., Senkowski, D., Soto-Faraco, S. & Woldorff, M.G. (2010) The multifaceted interplay between attention and multisensory integration. Trends Cogn. Sci., 14, 400-410.
53. Teder-Salejarvi, W.A., Di Russo, F., McDonald, J.J. & Hillyard, S.A. (2005) Effects of spatial congruity on audio-visual multimodal integration. J. Cognitive Neurosci., 17, 1396-1409.
54. Uddin, L.Q., Supekar, K.S., Ryali, S. & Menon, V. (2011) Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development. J. Neurosci., 31, 18578-18589.
55. Yago, E., Duarte, A., Wong, T., Barcelo, F. & Knight, R.T. (2004) Temporal kinetics of prefrontal modulation of the extrastriate cortex during visual attention. Cogn. Affect. Behav. Ne., 4, 609-617.