Skip to main content
Top
Published in: Brain Structure and Function 5-6/2010

01-06-2010 | Review

The hidden side of intentional action: the role of the anterior insular cortex

Authors: Marcel Brass, Patrick Haggard

Published in: Brain Structure and Function | Issue 5-6/2010

Login to get access

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.
Literature
go back to reference Ach N (1905) Über die Willenstätigkeit und das Denken: Eine experimentelle Untersuchung mit einem Anhange: Über das Hippsche Chronoskop. Vandenhoeck & Ruprecht, Göttingen Ach N (1905) Über die Willenstätigkeit und das Denken: Eine experimentelle Untersuchung mit einem Anhange: Über das Hippsche Chronoskop. Vandenhoeck & Ruprecht, Göttingen
go back to reference Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177CrossRefPubMed Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177CrossRefPubMed
go back to reference Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229–244CrossRefPubMed Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229–244CrossRefPubMed
go back to reference 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 10:682–694CrossRefPubMed 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 10:682–694CrossRefPubMed
go back to reference 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 309:488–491CrossRefPubMed 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 309:488–491CrossRefPubMed
go back to reference Blakemore SJ, Wolpert DM, Frith CD (1998) Central cancellation of self-produced tickle sensation. Nat Neurosci 1:635–640CrossRefPubMed Blakemore SJ, Wolpert DM, Frith CD (1998) Central cancellation of self-produced tickle sensation. Nat Neurosci 1:635–640CrossRefPubMed
go back to reference Brass M, Haggard P (2007) To do or not to do: the neural signature of self-control. J Neurosci 27:9141–9145CrossRefPubMed Brass M, Haggard P (2007) To do or not to do: the neural signature of self-control. J Neurosci 27:9141–9145CrossRefPubMed
go back to reference Brass M, Haggard P (2008) The what, when, whether model of intentional action. Neuroscientist 14:319–325CrossRefPubMed Brass M, Haggard P (2008) The what, when, whether model of intentional action. Neuroscientist 14:319–325CrossRefPubMed
go back to reference Campbell-Meiklejohn DK, Woolrich MW, Passingham RE, Rogers RD (2008) Knowing when to stop: the brain mechanisms of chasing losses. Biol Psychiatry 63:293–300CrossRefPubMed Campbell-Meiklejohn DK, Woolrich MW, Passingham RE, Rogers RD (2008) Knowing when to stop: the brain mechanisms of chasing losses. Biol Psychiatry 63:293–300CrossRefPubMed
go back to reference Chua HF, Gonzalez R, Taylor SF, Welsh RC, Liberzon I (2009) Decision-related loss: regret and disappointment. Neuroimage 47:2031–2040CrossRefPubMed Chua HF, Gonzalez R, Taylor SF, Welsh RC, Liberzon I (2009) Decision-related loss: regret and disappointment. Neuroimage 47:2031–2040CrossRefPubMed
go back to reference Clark L, Lawrence AJ, Astley-Jones F, Gray N (2009) Gambling near-misses enhance motivation to gamble and recruit win-related brain circuitry. Neuron 61:481–490CrossRefPubMed Clark L, Lawrence AJ, Astley-Jones F, Gray N (2009) Gambling near-misses enhance motivation to gamble and recruit win-related brain circuitry. Neuron 61:481–490CrossRefPubMed
go back to reference Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666PubMed Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666PubMed
go back to reference Craig AD (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505CrossRefPubMed Craig AD (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505CrossRefPubMed
go back to reference Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571CrossRefPubMed Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571CrossRefPubMed
go back to reference Craig AD (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70CrossRefPubMed Craig AD (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70CrossRefPubMed
go back to reference Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195CrossRefPubMed Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195CrossRefPubMed
go back to reference 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 15:373–385CrossRefPubMed 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 15:373–385CrossRefPubMed
go back to reference 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 132:843–852CrossRefPubMed 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 132:843–852CrossRefPubMed
go back to reference 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 40:1202–1213CrossRefPubMed 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 40:1202–1213CrossRefPubMed
go back to reference Desmurget M, Reilly KT, Richard N, Szathmari A, Mottolese C, Sirigu A (2009) Movement intention after parietal cortex stimulation in humans. Science 324:811–813CrossRefPubMed Desmurget M, Reilly KT, Richard N, Szathmari A, Mottolese C, Sirigu A (2009) Movement intention after parietal cortex stimulation in humans. Science 324:811–813CrossRefPubMed
go back to reference 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 28:9790–9796CrossRefPubMed 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 28:9790–9796CrossRefPubMed
go back to reference Fotopoulou A, Rudd A, Holmes P, Kopelman M (2009) Self-observation reinstates motor awareness in anosognosia for hemiplegia. Neuropsychologia 47:1256–1260CrossRefPubMed Fotopoulou A, Rudd A, Holmes P, Kopelman M (2009) Self-observation reinstates motor awareness in anosognosia for hemiplegia. Neuropsychologia 47:1256–1260CrossRefPubMed
go back to reference 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 11:3656–3666PubMed 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 11:3656–3666PubMed
go back to reference 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 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
go back to reference 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 130:1525–1537CrossRefPubMed 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 130:1525–1537CrossRefPubMed
go back to reference 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):913–933CrossRefPubMed 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):913–933CrossRefPubMed
go back to reference 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):1216–1228CrossRefPubMed 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):1216–1228CrossRefPubMed
go back to reference 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 (2010) Right insula for our sense of limb ownership and self-awareness of actions. Brain Struct Funct (this issue)
go back to reference Karnath HO, Baier B, Nagele T (2005) Awareness of the functioning of one’s own limbs mediated by the insular cortex? J Neurosci 25:7134–7138CrossRefPubMed Karnath HO, Baier B, Nagele T (2005) Awareness of the functioning of one’s own limbs mediated by the insular cortex? J Neurosci 25:7134–7138CrossRefPubMed
go back to reference 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 321:806–810CrossRefPubMed 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 321:806–810CrossRefPubMed
go back to reference Krieghoff V, Brass M, Prinz W, Waszak F (2009) Dissociating what and when of intentional actions. Front Hum Neurosci 3:3CrossRefPubMed Krieghoff V, Brass M, Prinz W, Waszak F (2009) Dissociating what and when of intentional actions. Front Hum Neurosci 3:3CrossRefPubMed
go back to reference Kuhn S, Brass M (2009) When doing nothing is an option: the neural correlates of deciding whether to act or not. Neuroimage 46:1187–1193CrossRefPubMed Kuhn S, Brass M (2009) When doing nothing is an option: the neural correlates of deciding whether to act or not. Neuroimage 46:1187–1193CrossRefPubMed
go back to reference Kuhn S, Haggard P, Brass M (2009) Intentional inhibition: how the “veto-area” exerts control. Hum Brain Mapp 30:2834–2843CrossRefPubMed Kuhn S, Haggard P, Brass M (2009) Intentional inhibition: how the “veto-area” exerts control. Hum Brain Mapp 30:2834–2843CrossRefPubMed
go back to reference Lau HC, Rogers RD, Ramnani N, Passingham RE (2004a) Willed action and attention to the selection of action. Neuroimage 21:1407–1415CrossRefPubMed Lau HC, Rogers RD, Ramnani N, Passingham RE (2004a) Willed action and attention to the selection of action. Neuroimage 21:1407–1415CrossRefPubMed
go back to reference Lau HC, Rogers RD, Haggard P, Passingham RE (2004b) Attention to intention. Science 303:1208–1210CrossRefPubMed Lau HC, Rogers RD, Haggard P, Passingham RE (2004b) Attention to intention. Science 303:1208–1210CrossRefPubMed
go back to reference Lau H, Rogers RD, Passingham RE (2006) Dissociating response selection and conflict in the medial frontal surface. NeuroImage 29:446–451CrossRefPubMed Lau H, Rogers RD, Passingham RE (2006) Dissociating response selection and conflict in the medial frontal surface. NeuroImage 29:446–451CrossRefPubMed
go back to reference Lau HC, Rogers RD, Passingham RE (2007) Manipulating the experienced onset of intention after action execution. J Cogn Neurosci 19:81–90CrossRefPubMed Lau HC, Rogers RD, Passingham RE (2007) Manipulating the experienced onset of intention after action execution. J Cogn Neurosci 19:81–90CrossRefPubMed
go back to reference 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):623–642CrossRefPubMed 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):623–642CrossRefPubMed
go back to reference Medford N, Critchley HD (2010) Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Struct Funct (this issue) Medford N, Critchley HD (2010) Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Struct Funct (this issue)
go back to reference Moore J, Haggard P (2008) Awareness of action: inference and prediction. Conscious Cogn 17:136–144CrossRefPubMed Moore J, Haggard P (2008) Awareness of action: inference and prediction. Conscious Cogn 17:136–144CrossRefPubMed
go back to reference Mueller VA, Brass M, Waszak F, Prinz W (2007) The role of the preSMA and the rostral cingulate zone in internally selected actions. Neuroimage 37:1354–1361CrossRefPubMed Mueller VA, Brass M, Waszak F, Prinz W (2007) The role of the preSMA and the rostral cingulate zone in internally selected actions. Neuroimage 37:1354–1361CrossRefPubMed
go back to reference Nachev P, Rees G, Parton A, Kennard C, Husain M (2005) Volition and conflict in human medial frontal cortex. Curr Biol 15:122–128CrossRefPubMed Nachev P, Rees G, Parton A, Kennard C, Husain M (2005) Volition and conflict in human medial frontal cortex. Curr Biol 15:122–128CrossRefPubMed
go back to reference Olausson H, Wessberg J, Morrison I, McGlone F, Vallbo A (2010) The neurophysiology of unmyelinated tactile afferents. Neurosci Biobehav Rev 34:185–191CrossRefPubMed Olausson H, Wessberg J, Morrison I, McGlone F, Vallbo A (2010) The neurophysiology of unmyelinated tactile afferents. Neurosci Biobehav Rev 34:185–191CrossRefPubMed
go back to reference 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 83:502–512CrossRefPubMed 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 83:502–512CrossRefPubMed
go back to reference 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 1105:143–154CrossRefPubMed 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 1105:143–154CrossRefPubMed
go back to reference Redgrave P, Gurney K, Reynolds J (2008) What is reinforced by phasic dopamine signals? Brain Res Rev 58:322–339CrossRefPubMed Redgrave P, Gurney K, Reynolds J (2008) What is reinforced by phasic dopamine signals? Brain Res Rev 58:322–339CrossRefPubMed
go back to reference 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 7:80–84CrossRefPubMed 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 7:80–84CrossRefPubMed
go back to reference Soon CS, Brass M, Heinze HJ, Haynes JD (2008) Unconscious determinants of free decisions in the human brain. Nat Neurosci 11:543–545CrossRefPubMed Soon CS, Brass M, Heinze HJ, Haynes JD (2008) Unconscious determinants of free decisions in the human brain. Nat Neurosci 11:543–545CrossRefPubMed
go back to reference 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 37:335–342CrossRefPubMed 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 37:335–342CrossRefPubMed
go back to reference 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 163:201–212CrossRefPubMed 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 163:201–212CrossRefPubMed
go back to reference 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) 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)
go back to reference van Eimeren T, Wolbers T, Munchau A, Buchel C, Weiller C, Siebner HR (2006) Implementation of visuospatial cues in response selection. Neuroimage 29:286–294CrossRefPubMed van Eimeren T, Wolbers T, Munchau A, Buchel C, Weiller C, Siebner HR (2006) Implementation of visuospatial cues in response selection. Neuroimage 29:286–294CrossRefPubMed
go back to reference 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 28:691–697CrossRefPubMed 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 28:691–697CrossRefPubMed
Metadata
Title
The hidden side of intentional action: the role of the anterior insular cortex
Authors
Marcel Brass
Patrick Haggard
Publication date
01-06-2010
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 5-6/2010
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-010-0269-6

Other articles of this Issue 5-6/2010

Brain Structure and Function 5-6/2010 Go to the issue