Skip to main content
Log in

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

  • Review
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

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

    Google Scholar 

  • Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177

    Article  PubMed  Google Scholar 

  • Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229–244

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Blakemore SJ, Wolpert DM, Frith CD (1998) Central cancellation of self-produced tickle sensation. Nat Neurosci 1:635–640

    Article  CAS  PubMed  Google Scholar 

  • Brass M, Haggard P (2007) To do or not to do: the neural signature of self-control. J Neurosci 27:9141–9145

    Article  CAS  PubMed  Google Scholar 

  • Brass M, Haggard P (2008) The what, when, whether model of intentional action. Neuroscientist 14:319–325

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Chua HF, Gonzalez R, Taylor SF, Welsh RC, Liberzon I (2009) Decision-related loss: regret and disappointment. Neuroimage 47:2031–2040

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666

    CAS  PubMed  Google Scholar 

  • Craig AD (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505

    Article  CAS  PubMed  Google Scholar 

  • Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571

    Article  PubMed  Google Scholar 

  • Craig AD (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70

    Article  CAS  PubMed  Google Scholar 

  • Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fotopoulou A, Rudd A, Holmes P, Kopelman M (2009) Self-observation reinstates motor awareness in anosognosia for hemiplegia. Neuropsychologia 47:1256–1260

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Haggard P (2008) Human volition: towards a neuroscience of will. Nat Rev Neurosci 9:934–946

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Krieghoff V, Brass M, Prinz W, Waszak F (2009) Dissociating what and when of intentional actions. Front Hum Neurosci 3:3

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kuhn S, Haggard P, Brass M (2009) Intentional inhibition: how the “veto-area” exerts control. Hum Brain Mapp 30:2834–2843

    Article  PubMed  Google Scholar 

  • Lau HC, Rogers RD, Ramnani N, Passingham RE (2004a) Willed action and attention to the selection of action. Neuroimage 21:1407–1415

    Article  CAS  PubMed  Google Scholar 

  • Lau HC, Rogers RD, Haggard P, Passingham RE (2004b) Attention to intention. Science 303:1208–1210

    Article  CAS  PubMed  Google Scholar 

  • Lau H, Rogers RD, Passingham RE (2006) Dissociating response selection and conflict in the medial frontal surface. NeuroImage 29:446–451

    Article  PubMed  Google Scholar 

  • Lau HC, Rogers RD, Passingham RE (2007) Manipulating the experienced onset of intention after action execution. J Cogn Neurosci 19:81–90

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Nachev P, Rees G, Parton A, Kennard C, Husain M (2005) Volition and conflict in human medial frontal cortex. Curr Biol 15:122–128

    Article  CAS  PubMed  Google Scholar 

  • Olausson H, Wessberg J, Morrison I, McGlone F, Vallbo A (2010) The neurophysiology of unmyelinated tactile afferents. Neurosci Biobehav Rev 34:185–191

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Redgrave P, Gurney K, Reynolds J (2008) What is reinforced by phasic dopamine signals? Brain Res Rev 58:322–339

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Soon CS, Brass M, Heinze HJ, Haynes JD (2008) Unconscious determinants of free decisions in the human brain. Nat Neurosci 11:543–545

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

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

Authors

Corresponding authors

Correspondence to Marcel Brass or Patrick Haggard.

Additional information

Both authors contributed equally to the current article.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-010-0269-6

Keywords

Navigation