Brain Structure and Function

, Volume 222, Issue 8, pp 3691–3703 | Cite as

The angular gyrus is a supramodal comparator area in action–outcome monitoring

  • Bianca M. van KemenadeEmail author
  • B. Ezgi Arikan
  • Tilo Kircher
  • Benjamin Straube
Original Article


Predicting and processing the sensory consequences of one’s own actions is essential to enable successful interactions with the environment. Previous studies have suggested that the angular gyrus detects discrepancies between predicted and actual action consequences, at least for unimodal feedback. However, most actions lead to multisensory consequences, raising the question whether previous models can sufficiently explain action–outcome processing. Here, we investigated neural comparator processes during detection of delays between action and unimodal or bimodal consequences in human subjects with fMRI, using parametric and connectivity analyses. Participants had to perform button presses, which led to the presentation of either a dot on the screen, a tone, or both, presented with a variable delay after the button press. Participants were asked to judge whether there was a delay between action and feedback. Activity in the angular gyrus correlated positively with delay for both visual, auditory, and audio-visual action consequences. Furthermore, the angular gyrus was functionally connected with midline structures such as the posterior cingulate cortex and precuneus in all conditions. Our results show that the angular gyrus is (1) a supramodal area, sensitive to delays in multiple modalities, and (2) functionally connected with self-referential areas during delay detection of both unimodal and bimodal action consequences. Overall, our results suggest that the angular gyrus functions as a mediator between perception and interpretation, and that this process is remarkably similar for unimodal and bimodal action consequences.


Voluntary action Forward model Delayed sensory feedback fMRI 



Data are available at doi: 10.5281/zenodo.556085. This study was funded by the “Deutsche Forschungsgemeinschaft” (DFG) through the SFB/Transregio 135, “Cardinal mechanisms of perception: prediction, valuation, categorization”, and through the International Research Training Group, IRTG 1901, “The Brain in Action-BrainAct”. BS is supported by DFG Grants STR 1146/8-1 and STR 1146/9-1. The authors declare no competing financial interests. We thank Jens Sommer and Kornelius Podranski for technical support, and Zeinab Helili for help with data collection.


  1. Blakemore S, Wolpert DM, Frith CD (1999) The cerebellum contributes to somatosensory cortical activity during self-produced tactile stimulation. NeuroImage 10:448–459CrossRefPubMedGoogle Scholar
  2. Blakemore S, Frith CD, Wolpert DM (2001) The cerebellum is involved in predicting the sensory consequences of action. NeuroReport 12(9):1879–1884CrossRefPubMedGoogle Scholar
  3. Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436CrossRefPubMedGoogle Scholar
  4. Cabanis M, Pyka M, Mehl S, Müller BW, Loos-jankowiak S, Winterer G et al (2013) The precuneus and the insula in self-attributional processes. Cognitive Affect Behav Neurosci 13:330–345. doi: 10.3758/s13415-012-0143-5 CrossRefGoogle Scholar
  5. David N, Cohen MX, Newen A, Bewernick BH, Shah NJ, Fink GR, Vogeley K (2007) The extrastriate cortex distinguishes between the consequences of one’s own and others’ behavior. NeuroImage 36:1004–1014. doi: 10.1016/j.neuroimage.2007.03.030 CrossRefPubMedGoogle Scholar
  6. Farrer C, Frith CD (2002) Experiencing oneself vs another person as being the cause of an action: the neural correlates of the experience of agency. NeuroImage 15:596–603. doi: 10.1006/nimg.2001.1009 CrossRefPubMedGoogle Scholar
  7. Farrer C, Franck N, Georgieff N, Frith CD, Decety J, Jeannerod M (2003) Modulating the experience of agency: a positron emission tomography study. NeuroImage 18:324–333. doi: 10.1016/S1053-8119(02)00041-1 CrossRefPubMedGoogle Scholar
  8. Farrer C, Frey SH, Van Horn JD, Tunik E, Turk D, Inati S, Grafton ST (2008) The angular gyrus computes action awareness representations. Cereb Cortex 18(2):254–261. doi: 10.1093/cercor/bhm050 CrossRefPubMedGoogle Scholar
  9. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19:1273–1302. doi: 10.1016/S1053-8119(03)00202-7 CrossRefPubMedGoogle Scholar
  10. Frund I, Haenel NV, Wichmann FA (2011) Inference for psychometric functions in the presence of nonstationary behavior. J Vis 11(6):16CrossRefPubMedGoogle Scholar
  11. Khalighinejad N, Haggard P (2015) Modulating human sense of agency with non-invasive brain stimulation. Cortex 69:93–103. doi: 10.1016/j.cortex.2015.04.015 CrossRefPubMedGoogle Scholar
  12. Kircher TTJ, Brammer M, Bullmore E, Simmons A, Bartels M, David AS (2002) The neural correlates of intentional and incidental self processing. Neuropsychologia 40:683–692CrossRefPubMedGoogle Scholar
  13. Kjaer TW, Nowak M, Lou HC (2002) Reflective self-awareness and conscious states: PET evidence for a common midline parietofrontal core. NeuroImage 1086:1080–1086. doi: 10.1006/nimg.2002.1230 CrossRefGoogle Scholar
  14. Laurienti PJ, Burdette JH, Wallace MT, Yen Y-F, Field AS, Stein BE (2002) Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci 14(3):420–429CrossRefPubMedGoogle Scholar
  15. Leube DT, Knoblich G, Erb M, Grodd W, Bartels M, Kircher TTJ (2003a) The neural correlates of perceiving one’s own movements. NeuroImage 20:2084–2090. doi: 10.1016/j.neuroimage.2003.07.033 CrossRefPubMedGoogle Scholar
  16. Leube DT, Knoblich G, Erb M, Kircher TTJ (2003b) Observing one’s hand become anarchic: an fMRI study of action identification. Conscious Cogn 12:597–608. doi: 10.1016/S1053-8100(03)00079-5 CrossRefPubMedGoogle Scholar
  17. Leube DT, Knoblich G, Erb M, Schlotterbeck P, Kircher TTJ (2010) The neural basis of disturbed efference copy mechanism in patients with schizophrenia. Cognitive Neurosci 1(2):111–117. doi: 10.1080/17588921003646156 CrossRefGoogle Scholar
  18. Maldjian JA, Laurienti PJ, Burdette JH, Kraft RA (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19:1233–1239. doi: 10.1016/S1053-8119(03)00169-1 CrossRefPubMedGoogle Scholar
  19. Miall RC, Wolpert DM (1996) Forward models for physiological motor control. Neural Netw 9(8):1265–1279. doi: 10.1016/S0893-6080(96)00035-4 CrossRefPubMedGoogle Scholar
  20. Mozolic JL, Joyner D, Hugenschmidt CE, Peiffer AM, Kraft RA, Maldjian JA, Laurienti PJ (2008) Cross-modal deactivations during modality-specific selective attention. BMC Neurol 8:35CrossRefPubMedPubMedCentralGoogle Scholar
  21. Nahab FB, Kundu P, Gallea C, Kakareka J, Pursley R, Pohida T et al (2011) The neural processes underlying self-agency. Cereb Cortex 1(21):48–55. doi: 10.1093/cercor/bhq059 CrossRefGoogle Scholar
  22. Nichols T, Brett M, Andersson J, Wager T, Poline JB (2005) Valid conjunction inference with the minimum statistic. NeuroImage 25:653–660CrossRefPubMedGoogle Scholar
  23. Northoff G, Heinzel A, Greck M De, Bermpohl F, Dobrowolny H, Panksepp J (2006) Self-referential processing in our brain—a meta-analysis of imaging studies on the self. NeuroImage 31:440–457. doi: 10.1016/j.neuroimage.2005.12.002 CrossRefPubMedGoogle Scholar
  24. Rohde M, Ernst M (2013) To lead and to lag–forward and backward recalibration of perceived visuo-motor simultaneity. Front Psychol 3:599CrossRefPubMedPubMedCentralGoogle Scholar
  25. Sperduti M, Delaveau P, Fossati P, Nadel J (2011) Different brain structures related to self- and external-agency attribution: a brief review and meta-analysis. Brain Struct Funct 216:151–157. doi: 10.1007/s00429-010-0298-1 CrossRefPubMedGoogle Scholar
  26. Sperry RW (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43:482–489CrossRefPubMedGoogle Scholar
  27. Stein BE, Stanford TR (2008) Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci. doi: 10.1038/nrn2331 PubMedGoogle Scholar
  28. Straube B, van Kemenade BM, Arikan BE, Fiehler K, Leube DT, Harris LR, Kircher T (2017) Predicting the multisensory consequences of one’s own action: BOLD suppression in auditory and visual cortices. PLoS One 12(1):e0169131. doi: 10.1371/JOURNAL.PONE.0169131 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Talsma D, Doty TJ, Woldorff MG (2007) Selective attention and audiovisual integration: is attending to both modalities a prerequisite for early integration? Cereb Cortex 17:679–690. doi: 10.1093/cercor/bhk016 CrossRefPubMedGoogle Scholar
  30. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 289:273–289. doi: 10.1006/nimg.2001.0978 CrossRefGoogle Scholar
  31. van Kemenade BM, Arikan BE, Kircher T, Straube B (2016) Predicting the sensory consequences of one’s own action: first evidence for multisensory facilitation. Atten Percept Psychophys. doi: 10.3758/s13414-016-1189-1 PubMedGoogle Scholar
  32. von Holst E, Mittelstaedt H (1950) Das reafferenzprinzip. Naturwissenschaften 37:464–476 [Translation of title: The principle of reafference] CrossRefGoogle Scholar
  33. Vroomen J, Keetels M (2010) Perception of intersensory synchrony: a tutorial review. Atten Percept Psychophys 72(4):871–884CrossRefPubMedGoogle Scholar
  34. Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11:R729–R732. doi: 10.1016/S0960-9822(01)00432-8 CrossRefPubMedGoogle Scholar
  35. Wolpert DM, Goodbody SJ, Husain M (1998) Maintaining internal representations: the role of the human superior parietal lobe. Nat Neurosci 1(6):529–533CrossRefPubMedGoogle Scholar
  36. Yomogida Y, Sugiura M, Sassa Y, Wakusawa K, Sekiguchi A, Fukushima A et al (2010) The neural basis of agency: an fMRI study. NeuroImage 50(1):198–207. doi: 10.1016/j.neuroimage.2009.12.054 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Psychiatry and PsychotherapyPhilipps-University MarburgMarburgGermany

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