Abstract
Anterior insular cortex is among the non-sensory brain regions most commonly found activated in functional brain imaging studies on visual and auditory perception. However, most of these studies do not explicitly address the functional role of this specific brain region in perception, but rather report its activation as a by-product. Here, we attempt to characterize the involvement of anterior insular cortex in various perceptual paradigms, including studies of visual awareness, perceptual decision making, cross-modal sensory processes and the role of spontaneous neural activity fluctuations in perception. We conclude that anterior insular cortex may be associated with perception in that it underpins heightened alertness of either stimulus- or task-driven origin, or both. Such a mechanism could integrate endogenous and exogenous functional demands under the joint criterion of whether they challenge an individual’s homeostasis.
Similar content being viewed by others
References
Amedi A, von Kriegstein K, van Atteveldt NM, Beauchamp MS, Naumer MJ (2005) Functional imaging of human crossmodal identification and object recognition. Exp Brain Res 166:559–571
Banati RB, Goerres GW, Tjoa C, Aggleton JP, Grasby P (2000) The functional anatomy of visual–tactile integration in man: a study using positron emission tomography. Neuropsychologia 38:115–124
Bartels A, Zeki S (2004) The neural correlates of maternal and romantic love. Neuroimage 21:1155–1166
Beck DM, Rees G, Frith CD, Lavie N (2001) Neural correlates of change detection and change blindness. Nat Neurosci 4:645–650
Benoit MM, Raij T, Lin FH, Jaaskelainen IP, Stufflebeam S (2009) Primary and multisensory cortical activity is correlated with audiovisual percepts. Hum Brain Mapp 31:526–538
Binder JR, Liebenthal E, Possing ET, Medler DA, Ward BD (2004) Neural correlates of sensory and decision processes in auditory object identification. Nat Neurosci 7:295–301
Boly M, Balteau E, Schnakers C, Degueldre C, Moonen G, Luxen A, Phillips C, Peigneux P, Maquet P, Laureys S (2007) Baseline brain activity fluctuations predict somatosensory perception in humans. Proc Natl Acad Sci USA 104:12187–12192
Bushara KO, Grafman J, Hallett M (2001) Neural correlates of auditory–visual stimulus onset asynchrony detection. J Neurosci 21:300–304
Bushara KO, Hanakawa T, Immisch I, Toma K, Kansaku K, Hallett M (2003) Neural correlates of cross-modal binding. Nat Neurosci 6:190–195
Calvert GA (2001) Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cereb Cortex 11:1110–1123
Carmel D, Lavie N, Rees G (2006) Conscious awareness of flicker in humans involves frontal and parietal cortex. Curr Biol 16:907–911
Christensen MS, Ramsoy TZ, Lund TE, Madsen KH, Rowe JB (2006) An fMRI study of the neural correlates of graded visual perception. Neuroimage 31:1711–1725
Cohen L, Dehaene S, Naccache L, Lehericy S, Dehaene-Lambertz G, Henaff MA, Michel F (2000) The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. Brain 123(Pt 2):291–307
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215
Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666
Craig AD (2009) How do you feel––now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70
Critchley HD (2005) Neural mechanisms of autonomic, affective, and cognitive integration. J Comp Neurol 493:154–166
Curtis CE, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7:415–423
Damasio AR (2003) Looking for Spinoza: joy, sorrow, and the feeling brain. Hartcourt, Orlando
de Vignemont F, Singer T (2006) The empathic brain: how, when and why? Trends Cogn Sci 10:435–441
Deary IJ, Simonotto E, Meyer M, Marshall A, Marshall I, Goddard N, Wardlaw JM (2004) The functional anatomy of inspection time: an event-related fMRI study. Neuroimage 22:1466–1479
Dehaene S, Naccache L, Cohen L, Bihan DL, Mangin JF, Poline JB, Riviere D (2001) Cerebral mechanisms of word masking and unconscious repetition priming. Nat Neurosci 4:752–758
Dosenbach NUF, Visscher KM, Palmer ED, Miezin FM, Wenger KK, Kang HC, Burgund ED, Grimes AL, Schlaggar BL, Petersen SE (2006) A core system for the implementation of task sets. Neuron 50:799–812
Dosenbach NUF, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RAT, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 104:11073–11078
Downar J, Crawley AP, Mikulis DJ, Davis KD (2000) A multimodal cortical network for the detection of changes in the sensory environment. Nat Neurosci 3:277–283
Eckert MA, Menon V, Walczak A, Ahlstrom J, Denslow S, Horwitz A, Dubno JR (2009) At the heart of the ventral attention system: the right anterior insula. Hum Brain Mapp 30:2530–2541
Eisenberger NI, Lieberman MD, Williams KD (2003) Does rejection hurt? An FMRI study of social exclusion. Science 302:290–292
Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711
Fox MD, Snyder AZ, Vincent JL, Raichle ME (2007) Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 56:171–184
Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19:1273–1302
Giraud AL, Kell C, Thierfelder C, Sterzer P, Russ MO, Preibisch C, Kleinschmidt A (2004) Contributions of sensory input, auditory search and verbal comprehension to cortical activity during speech processing. Cereb Cortex 14:247–255
Goebel R, Roebroeck A, Kim DS, Formisano E (2003) Investigating directed cortical interactions in time-resolved fMRI data using vector autoregressive modeling and Granger causality mapping. Magn Reson Imaging 21:1251–1261
Gold JI, Shadlen MN (2007) The neural basis of decision making. Annu Rev Neurosci 30:535–574
Grinband J, Hirsch J, Ferrera VP (2006) A neural representation of categorization uncertainty in the human brain. Neuron 49:757–763
Hadjikhani N, Roland PE (1998) Cross-modal transfer of information between the tactile and the visual representations in the human brain: a positron emission tomographic study. J Neurosci 18:1072–1084
Heekeren HR, Marrett S, Ungerleider LG (2008) The neural systems that mediate human perceptual decision making. Nat Rev Neurosci 9:467–479
Heimer L, Van Hoesen GW (2006) The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30:126–147
Hesselmann G, Kell CA, Kleinschmidt A (2008a) Ongoing activity fluctuations in hMT+ bias the perception of coherent visual motion. J Neurosci 28:14481–14485
Hesselmann G, Kell CA, Eger E, Kleinschmidt A (2008b) Spontaneous local variations in ongoing neural activity bias perceptual decisions. Proc Natl Acad Sci USA 105:10984–10989
Ho TC, Brown S, Serences JT (2009) Domain general mechanisms of perceptual decision making in human cortex. J Neurosci 29:8675–8687
Ivanoff J, Branning P, Marois R (2009) Mapping the pathways of information processing from sensation to action in four distinct sensorimotor tasks. Hum Brain Mapp 30:4167–4186
Jabbi M, Swart M, Keysers C (2007) Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 34:1744–1753
Kikyo H, Ohki K, Miyashita Y (2002) Neural correlates for feeling-of-knowing: an fMRI parametric analysis. Neuron 36:177–186
Kleinschmidt A, Buchel C, Hutton C, Friston KJ, Frackowiak RS (2002) The neural structures expressing perceptual hysteresis in visual letter recognition. Neuron 34:659–666
Kosillo P, Smith AT (2010) The role of the human anterior insular cortex in time processing. Brain Struct Funct. doi:10.1007/s00429-010-0267-8
Lumer L, Rees G (1999) Covariation of activity in visual and prefrontal cortex associated with subjective visual perception. Proc Natl Acad Sci 96:1669–1673
Makeig S, Inlow M (1993) Lapses in alertness: coherence of fluctuations in performance and EEG spectrum. Electroencephalogr Clin Neurophysiol 86:23–35
Manes F, Paradiso S, Springer JA, Lamberty G, Robinson RG (1999) Neglect after right insular cortex infarction. Stroke 30:946–948
Marois R, Chun MM, Gore JC (2000) Neural correlates of the attentional blink. Neuron 28:299–308
Marois R, Yi DJ, Chun MM (2004) The neural fate of consciously perceived and missed events in the attentional blink. Neuron 41:465–472
McGurk H, MacDonald J (1976) Hearing lips and seeing voices. Nature 264:746–748
Mesulam MM, Mufson EJ (1982) Insula of the old world monkey III: efferent cortical output and comments on function. J Comp Neurol 212:38–52
Miller LM, D’Esposito M (2005) Perceptual fusion and stimulus coincidence in the cross-modal integration of speech. J Neurosci 25:5884–5893
Mufson EJ, Mesulam MM (1982) Insula of the old world monkey II: afferent cortical input and comments on the claustrum. J Comp Neurol 212:23–37
Muller TJ, Federspiel A, Horn H, Lovblad K, Lehmann C, Dierks T, Strik WK (2005) The neurophysiological time pattern of illusionary visual perceptual transitions: a simultaneous EEG and fMRI study. Int J Psychophysiol 55:299–312
Nelson SM, Dosenbach NUF, Cohen AL, Schlaggar BL, Petersen SE (2010) Role of the anterior insula in task-level control and focal attention. Brain Struct Funct. doi:10.1007/s00429-010-0260-2
Penfield W, Faulk ME Jr (1955) The insula; further observations on its function. Brain 78:445–470
Pessoa L, Padmala S (2005) Quantitative prediction of perceptual decisions during near-threshold fear detection. Proc Natl Acad Sci USA 102:5612–5617
Pessoa L, Padmala S (2007) Decoding near-threshold perception of fear from distributed single-trial brain activation. Cereb Cortex 17:691–701
Peyron R, Laurent B, Garcia-Larrea L (2000) Functional imaging of brain responses to pain. A review, meta-analysis (2000). Neurophysiol Clin 30:263–288
Philiastides MG, Sajda P (2007) EEG-informed fMRI reveals spatiotemporal characteristics of perceptual decision making. J Neurosci 27:13082–13091
Ploran EJ, Nelson SM, Velanova K, Donaldson DI, Petersen SE, Wheeler ME (2007) Evidence accumulation and the moment of recognition: dissociating perceptual recognition processes using fMRI. J Neurosci 27:11912–11924
Rees G (2007) Neural correlates of the contents of visual awareness in humans. Philos Trans R Soc Lond B Biol Sci 362:877–886
Ridderinkhof KR, van den Wildenberg WP, Segalowitz SJ, Carter CS (2004) Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn 56:129–140
Sadaghiani S, Hesselmann G, Kleinschmidt A (2009) Distributed and antagonistic contributions of ongoing activity fluctuations to auditory stimulus detection. J Neurosci 29:13410–13417
Sahraie A, Weiskrantz L, Barbur JL, Simmons A, Williams SC, Brammer MJ (1997) Pattern of neuronal activity associated with conscious and unconscious processing of visual signals. Proc Natl Acad Sci USA 94:9406–9411
Saper CB (2002) The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu Rev Neurosci 25:433–469
Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356
Sekuler R, Sekuler AB, Lau R (1997) Sound alters visual motion perception. Nature 385:308
Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci USA 106:13040–13045
Sporns O, Honey CJ, Kotter R (2007) Identification and classification of hubs in brain networks. PLoS One 2:e1049
Sridharan D, Levitin DJ, 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
Sterzer P, Kleinschmidt A (2007) A neural basis for inference in perceptual ambiguity. Proc Natl Acad Sci 104:323–328
Sterzer P, Stadler C, Poustka F, Kleinschmidt A (2007) A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy. Neuroimage 37:335–342
Sterzer P, Kleinschmidt A, Rees G (2009) The neural bases of multistable perception. Trends Cogn Sci 13:310–318
Sturm W, Longoni F, Fimm B, Dietrich T, Weis S, Kemna S, Herzog H, Willmes K (2004) Network for auditory intrinsic alertness: a PET study. Neuropsychologia 42:563–568
Taylor KS, Seminowicz DA, Davis KD (2009) Two systems of resting state connectivity between the insula and cingulate cortex. Hum Brain Mapp 30:2731–2745
Thielscher A, Pessoa L (2007) Neural correlates of perceptual choice and decision making during fear–disgust discrimination. J Neurosci 27:2908–2917
Vincent JL, Kahn I, Snyder AZ, Raichle ME, Buckner RL (2008) Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J Neurophysiol 100:3328–3342
Acknowledgments
We thank Sepideh Sadaghiani for helpful comments on the manuscript. AK received support from the Agence Nationale de la Recherche (SPONTACT grant) and PS from the German Research Foundation (Emmy-Noether Programme).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sterzer, P., Kleinschmidt, A. Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct Funct 214, 611–622 (2010). https://doi.org/10.1007/s00429-010-0252-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-010-0252-2