Brain Structure and Function

, Volume 223, Issue 3, pp 1343–1355 | Cite as

Brain waves from an “isolated” cortex: contribution of the anterior insula to cognitive functions

  • Rinaldo Livio Perri
  • Marika Berchicci
  • Valentina Bianco
  • Donatella Spinelli
  • Francesco Di Russo
Original Article


Using two independent electrical neuroimaging techniques (BESA and sLORETA), we tested a fMRI-seeded source modeling indicating that in visual discriminative tasks the anterior insula (aIns) participates in the generation of three prefrontal ERP components: the pN1 (at 115 ms), the pP1 (at 170 ms), and the pP2 (at 300 ms). This latter component represented the focus of the present study. Results showed that the pP2 had different activation profiles across hemispheres. The left aIns activity peaked at 420 ms (30 ms before the response) for both Go and No-go trials, that is independently from the ultimate choice (response or inhibition). The right aIns activity started at about 250 ms and progressively increased for a time interval extending after the motor response; its amplitude was larger in case of Go than No-go stimuli. We suggest that the activation of the left aIns reflected the timing of the decision, and the right aIns the categorization and the performance monitoring processes. A control experiment requiring simple (not discriminative) motor response revealed that the pP2 and the aIns activity were nearly absent after the 250 ms; this result confirmed that the aIns activity at this stage is associated with the decisional processes, and not with the motor response per se. The present investigation shed new lights on the insular contribution to perceptual decision-making, and opens to the possibility of assessing the aIns activity via ERP analysis.


ERP BESA sLORETA Anterior insula Decision-making 


  1. Berchicci M, Lucci G, Perri RL, Spinelli D, Di Russo F (2014) Benefits of physical exercise on basic visuo-motor functions across age. Front Aging Neurosci 6:48CrossRefPubMedPubMedCentralGoogle Scholar
  2. Berchicci M, Spinelli D, Di Russo F (2016) New insights about old waves. Stimulus- and response-locked ERPs on the same time-window. Biol Psychol 117:202–215CrossRefPubMedGoogle Scholar
  3. 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(3):295–301CrossRefPubMedGoogle Scholar
  4. Böcker KB, Brunia CH, van den Berg-Lenssen MM (1994) A spatiotemporal dipole model of the stimulus preceding negativity (SPN) prior to feedback stimuli. Brain Topogr 7(1):71–88CrossRefPubMedGoogle Scholar
  5. Boettiger CA, D’Esposito M (2005) Frontal networks for learning and executing arbitrary stimulus-response associations. J Neurosci 25(10):2723–2732CrossRefPubMedGoogle Scholar
  6. Chang LJ, Yarkoni T, Khaw MW, Sanfey AG (2013) Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb Cortex 23(3):739–749CrossRefPubMedGoogle Scholar
  7. Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3(8):655–666CrossRefPubMedGoogle Scholar
  8. Craig AD (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13(4):500–505CrossRefPubMedGoogle Scholar
  9. Craig AD (2009a) How do you feel—now? the anterior insula and human awareness. Nat Rev Neurosci 10(1):59–70CrossRefPubMedGoogle Scholar
  10. Craig AD (2009b) Emotional moments across time: a possible neural basis for time perception in the anterior insula. Philos Trans Biol Sci 364:1933–1942CrossRefGoogle Scholar
  11. Damasio A (2003) Feelings of emotion and the self. Ann N Y Acad Sci 1001(1):253–261CrossRefPubMedGoogle Scholar
  12. Di Rollo A, Cosottini M, Pesaresi I, Fabbri S, Di Russo F, Perri RL, Sartucci F (2016) ERP generators in an omitted-target oddball task: a simultaneous EEG-fMRI study. Clin Neurophysiol 127(12):e330CrossRefGoogle Scholar
  13. Di Russo F, Pitzalis S (2013) EEG-fMRI combination for the study of visual perception and spatial attention. In: Cognitive electrophysiology of attention: signals of the mind. Academic Press, New York, pp 58–70Google Scholar
  14. Di Russo F, Martínez A, Sereno MI, Pitzalis S, Hillyard SA (2002) Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp 15(2):95–111CrossRefPubMedGoogle Scholar
  15. Di Russo F, Martínez A, Hillyard SA (2003) Source analysis of event-related cortical activity during visuo-spatial attention. Cereb Cortex 13(5):486–499CrossRefPubMedGoogle Scholar
  16. Di Russo F, Berchicci M, Perri RL, Ripani FR, Ripani M (2013) A passive exoskeleton can push your life up: application on multiple sclerosis patients. PLoS One 8(10):e77348CrossRefPubMedPubMedCentralGoogle Scholar
  17. Di Russo F, Lucci G, Sulpizio V, Berchicci M, Spinelli D, Pitzalis S, Galati G (2016) Spatiotemporal brain mapping during preparation, perception, and action. NeuroImage 126:1–14CrossRefPubMedGoogle Scholar
  18. Di Russo F, Berchicci M, Bozzacchi C, Perri RL, Pitzalis S, Spinelli D (2017) Beyond the “Bereitschaftspotential”: action preparation behind cognitive functions. Neurosci Biobehav Rev 78:57–81CrossRefPubMedGoogle Scholar
  19. Droutman V, Bechara A, Read SJ (2015) Roles of the different sub-regions of the insular cortex in various phases of the decision-making process. Front Behav Neurosci 9:309CrossRefPubMedPubMedCentralGoogle Scholar
  20. Feinstein JS, Stein MB, Paulus MP (2006) Anterior insula reactivity during certain decisions is associated with neuroticism. Soc Cogn Affect Neurosci 1(2):136–142CrossRefPubMedPubMedCentralGoogle Scholar
  21. Flynn FG (1999) Anatomy of the insula functional and clinical correlates. Aphasiology 13:55–78CrossRefGoogle Scholar
  22. Gajewski PD, Falkenstein M (2013) Effects of task complexity on ERP components in Go/No-go tasks. Int J Psychophysiol 87(3):273–278CrossRefPubMedGoogle Scholar
  23. Grech R, Cassar T, Muscat J, Camilleri KP, Fabri SG, Zervakis M, Vanrumste B (2008) Review on solving the inverse problem in EEG source analysis. J Neuroeng Rehabil 5(1):25CrossRefPubMedPubMedCentralGoogle Scholar
  24. Grinband J, Hirsch J, Ferrera VP (2006) A neural representation of categorization uncertainty in the human brain. Neuron 49(5):757–763CrossRefPubMedGoogle Scholar
  25. Hall DA, Haggard MP, Akeroyd MA, Summerfield AQ, Palmer AR, Elliott MR, Bowtell RW (2000) Modulation and task effects in auditory processing measured using fMRI. Hum Brain Mapp 10(3):107–119CrossRefPubMedGoogle Scholar
  26. Hampton AN, O’Doherty JP (2007) Decoding the neural substrates of reward-related decision making with functional MRI. Proc Natl Acad Sci 104(4):1377–1382CrossRefPubMedPubMedCentralGoogle Scholar
  27. Ho TC, Brown S, Serences JT (2009) Domain general mechanisms of perceptual decision making in human cortex. J Neurosci 29(27):8675–8687CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hoffmann S, Falkenstein M (2008) The correction of eye blink artefacts in the EEG: a comparison of two prominent methods. PLoS One 3(8):e3004CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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(12):4167–4186CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jung TP, Makeig S, Humphries C, Lee TW, Mckeown MJ, Iragui V, Sejnowski TJ (2000) Removing electroencephalographic artifacts by blind source separation. Psychophysiology 37(02):163–178CrossRefPubMedGoogle Scholar
  31. Kenemans JL, Kok A, Smulders FTY (1993) Event-related potentials to conjunctions of spatial frequency and orientation as a function of stimulus parameters and response requirements. Electroencephalogr Clin Neurophysiol 88(1):51–63CrossRefPubMedGoogle Scholar
  32. Lamichhane B, Dhamala M (2015) The salience network and its functional architecture in a perceptual decision: an effective connectivity study. Brain Connect 5(6):362–370CrossRefPubMedGoogle Scholar
  33. Lamichhane B, Adhikari BM, Dhamala M (2016) The activity in the anterior insulae is modulated by perceptual decision-making difficulty. Neuroscience 327:79–94CrossRefPubMedGoogle Scholar
  34. Lewis JW, Beauchamp MS, DeYoe EA (2000) A comparison of visual and auditory motion processing in human cerebral cortex. Cereb Cortex 10(9):873–888CrossRefPubMedGoogle Scholar
  35. Liu T, Pleskac TJ (2011) Neural correlates of evidence accumulation in a perceptual decision task. J Neurophysiol 106(5):2383–2398CrossRefPubMedGoogle Scholar
  36. Makeig S, Westerfield M, Jung TP, Covington J, Townsend J, Sejnowski TJ, Courchesne E (1999) Functionally independent components of the late positive event-related potential during visual spatial attention. J Neurosci 19(7):2665–2680PubMedGoogle Scholar
  37. Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, de Peralta RG (2004) EEG source imaging. Clin Neurophysiol 115(10):2195–2222CrossRefPubMedGoogle Scholar
  38. Nieuwenhuys R (2011) The insular cortex: a review. Prog Brain Res 195:123–163CrossRefGoogle Scholar
  39. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 104:199–206Google Scholar
  40. Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12PubMedGoogle Scholar
  41. Pascual-Marqui RD, Michel CM, Lehmann D (1994) Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int J Psychophysiol 18(1):49–65CrossRefPubMedGoogle Scholar
  42. Perri RL, Berchicci M, Spinelli D, Di Russo F (2014) Individual differences in response speed and accuracy are associated to specific brain activities of two interacting systems. Front Behav Neurosci 8:251PubMedPubMedCentralGoogle Scholar
  43. Perri RL, Berchicci M, Lucci G, Spinelli D, Di Russo F (2015) Why do we make mistakes? Neurocognitive processes during the preparation-perception-action cycle and error-detection. Neuroimage 113:320–328CrossRefPubMedGoogle Scholar
  44. Perri RL, Berchicci M, Lucci G, Spinelli D, Di Russo F (2016) How the brain prevents a second error in a perceptual decision-making task. Sci Rep 6:32058CrossRefPubMedPubMedCentralGoogle Scholar
  45. Perri RL, Spinelli D, Di Russo F (2017) Missing the target: the neural processing underlying the omission error. Brain Topogr 30(3):352–363CrossRefPubMedGoogle Scholar
  46. Pitzalis S, Strappini F, De Gasperis M, Bultrini A, Di Russo F (2012) Spatio-temporal brain mapping of motion-onset VEPs combined with fMRI and retinotopic maps. PLoS One 7(4):e35771CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pizzagalli DA, Oakes TR, Fox AS, Chung MK, Larson CL, Abercrombie HC, Davidson RJ (2004) Functional but not structural subgenual prefrontal cortex abnormalities in melancholia. Mol Psychiatry 9(4):393–405CrossRefGoogle Scholar
  48. 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(44):11912–11924CrossRefPubMedGoogle Scholar
  49. Ploran EJ, Tremel JJ, Nelson SM, Wheeler ME (2011) High quality but limited quantity perceptual evidence produces neural accumulation in frontal and parietal cortex. Cereb Cortex 21(11):2650–2662CrossRefPubMedPubMedCentralGoogle Scholar
  50. Potts GF, Tucker DM (2001) Frontal evaluation and posterior representation in target detection. Cogn Brain Res 11(1):147–156CrossRefGoogle Scholar
  51. Potts GF, Liotti M, Tucker DM, Posner MI (1996) Frontal and inferior temporal cortical activity in visual target detection: evidence from high spatially sampled event-related potentials. Brain Topogr 9(1):3–14CrossRefGoogle Scholar
  52. Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD (2003) The neural basis of economic decision-making in the ultimatum game. Science 300(5626):1755–1758CrossRefPubMedGoogle Scholar
  53. Sterzer P, Kleinschmidt A (2010) Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct Funct 214(5–6):611–622CrossRefPubMedGoogle Scholar
  54. Sulpizio V, Lucci G, Berchicci M, Galati G, Pitzalis S, Di Russo F (2017) Hemispheric asymmetries in the transition from action preparation to execution. NeuroImage 148:390–402CrossRefPubMedGoogle Scholar
  55. Thielscher A, Pessoa L (2007) Neural correlates of perceptual choice and decision making during fear–disgust discrimination. J Neurosci 27(11):2908–2917CrossRefPubMedGoogle Scholar
  56. Uddin LQ, Supekar K, Amin H, Rykhlevskaia E, Nguyen DA, Greicius MD, Menon V (2010) Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cereb Cortex 20:2636–2646CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ullsperger M, Harsay HA, Wessel JR, Ridderinkhof KR (2010) Conscious perception of errors and its relation to the anterior insula. Brain Struct Funct 214(5–6):629–643CrossRefPubMedPubMedCentralGoogle Scholar
  58. van Eimeren T, Wolbers T, Münchau A, Büchel C, Weiller C, Siebner HR (2006) Implementation of visuospatial cues in response selection. Neuroimage 29(1):286–294CrossRefPubMedGoogle Scholar
  59. Wheeler ME, Woo SG, Ansel T, Tremel JJ, Collier AL, Velanova K, Yang T (2015) The strength of gradually accruing probabilistic evidence modulates brain activity during a categorical decision. J Cogn Neurosci 27(4):705–719CrossRefPubMedGoogle Scholar
  60. Worrell GA, Lagerlund TD, Sharbrough FW, Brinkmann BH, Busacker NE, Cicora KM, O’Brien TJ (2000) Localization of the epileptic focus by low-resolution electromagnetic tomography in patients with a lesion demonstrated by MRI. Brain Topogr 12(4):273–282CrossRefPubMedGoogle Scholar
  61. Zumsteg D, Friedman A, Wieser HG, Wennberg RA (2006) Propagation of interictal discharges in temporal lobe epilepsy: correlation of spatiotemporal mapping with intracranial foramen ovale electrode recordings. Clin Neurophysiol 117(12):2615–2626CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Rinaldo Livio Perri
    • 1
    • 2
  • Marika Berchicci
    • 1
  • Valentina Bianco
    • 1
  • Donatella Spinelli
    • 1
    • 3
  • Francesco Di Russo
    • 1
    • 3
  1. 1.Department of Movement, Human and Health SciencesUniversity of Rome “Foro Italico”RomeItaly
  2. 2.University Niccolò CusanoRomeItaly
  3. 3.IRCCS Santa Lucia FoundationRomeItaly

Personalised recommendations