Abstract
Cognitive neuroscience research has begun to reveal the functional neuroanatomy of intentional action. This research has primarily pointed to the role of the medial frontal cortex for the voluntary control of behaviour. However, a closer inspection of the literature reveals that the anterior insular cortex (AIC) is also routinely activated in tasks that involve different aspects of intentional action. In the present article, we outline studies that have found AIC activation in various intentional action paradigms. Based on these findings, we discuss two hypotheses about the AIC’s contribution to voluntary control. One hypothesis states that AIC is involved in forming intentions, by providing information about the internal states of the system. The alternative view suggests that AIC evaluates the outcomes of intentional action decisions that have been previously formed elsewhere. The limited evidence so far favours the evaluative hypothesis. AIC may provide interoceptive signals that play an essential role in evaluating the consequences of intentional action. AIC is therefore a key structure for the adaptive, affective training of the individual will, on which human society depends.
Similar content being viewed by others
References
Ach N (1905) Über die Willenstätigkeit und das Denken: Eine experimentelle Untersuchung mit einem Anhange: Über das Hippsche Chronoskop. Vandenhoeck & Ruprecht, Göttingen
Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177
Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229–244
Ball T, Schreiber A, Feige B, Wagner M, Lucking CH, Kristeva-Feige R (1999) The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage 10:682–694
Berti A, Bottini G, Gandola M, Pia L, Smania N, Stracciari A, Castiglioni I, Vallar G, Paulesu E (2005) Shared cortical anatomy for motor awareness and motor control. Science 309:488–491
Blakemore SJ, Wolpert DM, Frith CD (1998) Central cancellation of self-produced tickle sensation. Nat Neurosci 1:635–640
Brass M, Haggard P (2007) To do or not to do: the neural signature of self-control. J Neurosci 27:9141–9145
Brass M, Haggard P (2008) The what, when, whether model of intentional action. Neuroscientist 14:319–325
Campbell-Meiklejohn DK, Woolrich MW, Passingham RE, Rogers RD (2008) Knowing when to stop: the brain mechanisms of chasing losses. Biol Psychiatry 63:293–300
Chua HF, Gonzalez R, Taylor SF, Welsh RC, Liberzon I (2009) Decision-related loss: regret and disappointment. Neuroimage 47:2031–2040
Clark L, Lawrence AJ, Astley-Jones F, Gray N (2009) Gambling near-misses enhance motivation to gamble and recruit win-related brain circuitry. Neuron 61:481–490
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 (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505
Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571
Craig AD (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70
Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195
Cunnington R, Windischberger C, Deecke L, Moser E (2002) The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. Neuroimage 15:373–385
De Brito SA, Mechelli A, Wilke M, Laurens KR, Jones AP, Barker GJ, Hodgins S, Viding E (2009) Size matters: increased grey matter in boys with conduct problems and callous-unemotional traits. Brain 132:843–852
de Oliveira-Souza R, Hare RD, Bramati IE, Garrido GJ, Azevedo Ignacio F, Tovar-Moll F, Moll J (2008) Psychopathy as a disorder of the moral brain: fronto-temporo-limbic grey matter reductions demonstrated by voxel-based morphometry. Neuroimage 40:1202–1213
Desmurget M, Reilly KT, Richard N, Szathmari A, Mottolese C, Sirigu A (2009) Movement intention after parietal cortex stimulation in humans. Science 324:811–813
Forstmann BU, Jahfari S, Scholte HS, Wolfensteller U, van den Wildenberg WP, Ridderinkhof KR (2008) Function and structure of the right inferior frontal cortex predict individual differences in response inhibition: a model-based approach. J Neurosci 28:9790–9796
Fotopoulou A, Rudd A, Holmes P, Kopelman M (2009) Self-observation reinstates motor awareness in anosognosia for hemiplegia. Neuropsychologia 47:1256–1260
Fried I, Katz A, McCarthy G, Sass KJ, Williamson P, Spencer SS, Spencer DD (1991) Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci 11:3656–3666
Haggard P (2008) Human volition: towards a neuroscience of will. Nat Rev Neurosci 9:934–946
Herwig A, Prinz W, Waszak F (2007) Two modes of sensorimotor integration in intention-based and stimulus-based actions. Q J Exp Psychol (Colchester) 60:1540–1554
Hodgson T, Chamberlain M, Parris B, James M, Gutowski N, Husain M, Kennard C (2007) The role of the ventrolateral frontal cortex in inhibitory oculomotor control. Brain 130:1525–1537
Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118(pt 4):913–933
Jenkins IH, Jahanshahi M, Jueptner M, Passingham RE, Brooks DJ (2000) Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. Brain 123(Pt 6):1216–1228
Karnath HO, Baier B (2010) Right insula for our sense of limb ownership and self-awareness of actions. Brain Struct Funct (this issue)
Karnath HO, Baier B, Nagele T (2005) Awareness of the functioning of one’s own limbs mediated by the insular cortex? J Neurosci 25:7134–7138
King-Casas B, Sharp C, Lomax-Bream L, Lohrenz T, Fonagy P, Montague PR (2008) The rupture and repair of cooperation in borderline personality disorder. Science 321:806–810
Krieghoff V, Brass M, Prinz W, Waszak F (2009) Dissociating what and when of intentional actions. Front Hum Neurosci 3:3
Kuhn S, Brass M (2009) When doing nothing is an option: the neural correlates of deciding whether to act or not. Neuroimage 46:1187–1193
Kuhn S, Haggard P, Brass M (2009) Intentional inhibition: how the “veto-area” exerts control. Hum Brain Mapp 30:2834–2843
Lau HC, Rogers RD, Ramnani N, Passingham RE (2004a) Willed action and attention to the selection of action. Neuroimage 21:1407–1415
Lau HC, Rogers RD, Haggard P, Passingham RE (2004b) Attention to intention. Science 303:1208–1210
Lau H, Rogers RD, Passingham RE (2006) Dissociating response selection and conflict in the medial frontal surface. NeuroImage 29:446–451
Lau HC, Rogers RD, Passingham RE (2007) Manipulating the experienced onset of intention after action execution. J Cogn Neurosci 19:81–90
Libet B, Gleason CA, Wright EW, Pearl DK (1983) Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 106(Pt 3):623–642
Medford N, Critchley HD (2010) Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Struct Funct (this issue)
Moore J, Haggard P (2008) Awareness of action: inference and prediction. Conscious Cogn 17:136–144
Mueller VA, Brass M, Waszak F, Prinz W (2007) The role of the preSMA and the rostral cingulate zone in internally selected actions. Neuroimage 37:1354–1361
Nachev P, Rees G, Parton A, Kennard C, Husain M (2005) Volition and conflict in human medial frontal cortex. Curr Biol 15:122–128
Olausson H, Wessberg J, Morrison I, McGlone F, Vallbo A (2010) The neurophysiology of unmyelinated tactile afferents. Neurosci Biobehav Rev 34:185–191
Paulignan Y, MacKenzie C, Marteniuk R, Jeannerod M (1991) Selective perturbation of visual input during prehension movements. 1. The effects of changing object position. Exp Brain Res 83:502–512
Ramautar JR, Slagter HA, Kok A, Ridderinkhof KR (2006) Probability effects in the stop-signal paradigm: the insula and the significance of failed inhibition. Brain Res 1105:143–154
Redgrave P, Gurney K, Reynolds J (2008) What is reinforced by phasic dopamine signals? Brain Res Rev 58:322–339
Sirigu A, Daprati E, Ciancia S, Giraux P, Nighoghossian N, Posada A, Haggard P (2004) Altered awareness of voluntary action after damage to the parietal cortex. Nat Neurosci 7:80–84
Soon CS, Brass M, Heinze HJ, Haynes JD (2008) Unconscious determinants of free decisions in the human brain. Nat Neurosci 11:543–545
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
Tiihonen J, Rossi R, Laakso MP, Hodgins S, Testa C, Perez J, Repo-Tiihonen E, Vaurio O, Soininen H, Aronen HJ, Kononen M, Thompson PM, Frisoni GB (2008) Brain anatomy of persistent violent offenders: more rather than less. Psychiatry Res 163:201–212
Ullsperger M, Harsay HA, Wessel JR, Ridderinkhof KR (2010) Conscious perception of errors and its relation to the anterior insula. Brain Struct Funct (this issue)
van Eimeren T, Wolbers T, Munchau A, Buchel C, Weiller C, Siebner HR (2006) Implementation of visuospatial cues in response selection. Neuroimage 29:286–294
Wiese H, Stude P, Nebel K, Forsting M, de Greiff A (2005) Prefrontal cortex activity in self-initiated movements is condition-specific, but not movement-related. Neuroimage 28:691–697
Acknowledgments
PH was supported by a Leverhulme Trust Research Fellowship, and by project grants from ESRC and BBSRC. MB was supported by the Special Research Fund of Ghent University (BOF).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Both authors contributed equally to the current article.
Rights and permissions
About this article
Cite this article
Brass, M., Haggard, P. The hidden side of intentional action: the role of the anterior insular cortex. Brain Struct Funct 214, 603–610 (2010). https://doi.org/10.1007/s00429-010-0269-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-010-0269-6