Abstract
The way the brain controls voluntary movements for normal and pathological subject remains puzzling. In this selective review, we provide unreported harmonies between the anterior midcingulate cortex (aMCC) activities and the ideomotor mechanism postulating that voluntary movements are controlled by the anticipation of the expected perceptual consequences of an action, critically involving bidirectional interplay of a given motor activity and corresponding sensory feedback. Among other evidence, we found that the required asymmetry in the bidirectional interplay between a given motor command and its expected sensory effect could rely on the specific activity of aMCC neurons when observing errors and successes. We confirm this hypothesis by presenting a pathological perspective, studying obsessive–compulsive and other related disorders in which hyperactivated and uniform aMCC activities should lead to a circular-reflex process that results in persistent ideas and repeated actions. By evaluating normal and pathological data, we propose considering the aMCC at a central position within the cerebral network involved in the ideomotor mechanism.
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References
American-Psychiatric-Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Association, Arlington
Amiez C, Petrides M (2014) Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas. Cereb Cortex 24:563–578
Amiez C, Neveu R, Warrot D, Petrides M, Knoblauch K, Procyk E (2013) The location of feedback-related activity in the midcingulate cortex is predicted by local morphology. J Neurosci 33:2217–2228
Badets A, Osiurak F (2015) A goal-based mechanism for delayed motor intention: considerations from motor skills, tool use and action memory. Psychol Res 79:345–360. https://doi.org/10.1007/s00426-014-0581-5
Badets A, Osiurak F (2017) The ideomotor recycling theory for tool use, language, and foresight. Exp Brain Res 235:365–377. https://doi.org/10.1007/s00221-016-4812-4
Badets A, Koch I, Toussaint L (2013) Role of an ideomotor mechanism in number processing. Exp Psychol 60:34–43. https://doi.org/10.1027/1618-3169/a000171
Badets A, Koch I, Philipp AM (2016) A review of ideomotor approaches to perception, cognition, action, and language: advancing a cultural recycling hypothesis. Psychol Res 80:1–15. https://doi.org/10.1007/s00426-014-0643-8
Banca P, Voon V, Vestergaard MD et al (2015) Imbalance in habitual versus goal directed neural systems during symptom provocation in obsessive-compulsive disorder. Brain 138:798–811. https://doi.org/10.1093/brain/awu379
Bancaud J, Talairach J, Geier S, Bonis A, Trottier S, Manrique M (1976) Behavioral manifestations induced by electric stimulation of the anterior cingulate gyrus in man. Rev Neurol 132:705–724
Band GPH, Van Steenbergen H, Ridderinkhof KR, Falkenstein M, Hommel B (2009) Action-effect negativity: irrelevant action effects are monitored like relevant feedback. Biol Psychol 82:211–218. https://doi.org/10.1016/j.biopsycho.2009.06.011
Bosc M, Bioulac B, Langbour N et al (2017) Checking behavior in rhesus monkeys is related to anxiety and frontal activity. Sci Rep 7:45267. https://doi.org/10.1038/srep45267
Brandt VC, Lynn MT, Obst M, Brass M, Münchau A (2015) Visual feedback of own tics increases tic frequency in patients with Tourette's syndrome. Cogn Neurosci 6:1–7. https://doi.org/10.1080/17588928.2014.954990
Campbell MEJ, Mehrkanoon S, Cunnington R (2018) Intentionally not imitating: Insula cortex engaged for top-down control of action mirroring. Neuropsychologia 111:241–251. https://doi.org/10.1016/j.neuropsychologia.2018.01.037
Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747–749
Chassagnon S, Minotti L, Kremer S, Hoffmann D, Kahane P (2008) Somatosensory, motor, and reaching/grasping responses to direct electrical stimulation of the human cingulate motor areas. J Neurosurg 109:593–604. https://doi.org/10.3171/JNS/2008/109/10/0593
Coles ME, Heimberg RG, Frost RO, Steketee G (2005) Not just right experiences and obsessive-compulsive features: experimental and self-monitoring perspectives. Behav Res Ther 43:153–167. https://doi.org/10.1016/j.brat.2004.01.002
Colton J, Bach P, Whalley B, Mitchell C (2018) Intention insertion: activating an action’s perceptual consequences is sufficient to induce non-willed motor behavior. J Exp Psychol Gen 147:1256–1263. https://doi.org/10.1037/xge0000435
Critchley HD, Mathias CJ, Josephs O et al (2003) Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126:2139–2152. https://doi.org/10.1093/brain/awg216
Damasio AR (1996) The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos Trans R Soc Lond B 351:1413–1420. https://doi.org/10.1098/rstb.1996.0125
Debener S, Ullsperger M, Siegel M, Fiehler K, von Cramon DY, Engel AK (2005) Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J Neurosci 25:11730–11737
Dehaene S, Posner MI, Tucker DM (1994) Localization of a neural system for error detection and compensation. Psychol Sci 5:303–305
Dehaene S, Artiges E, Naccache L et al (2003) Conscious and subliminal conflicts in normal subjects and patients with schizophrenia: the role of the anterior cingulate. Proc Natl Acad Sci 100:13722–13727. https://doi.org/10.1073/pnas.2235214100
Deiber MP, Honda M, Ibañez V, Sadato N, Hallett M (1999) Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. J Neurophysiol 81:3065–3077. https://doi.org/10.1152/jn.1999.81.6.3065
Devinsky O, Luciano D (1993) The contributions of cingulate cortex to human behavior. In: Vogt BABA, Gabriel M (eds) Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook. Birkhäuser, Boston, pp 527–556
Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306
Dogge M, Custers R, Aarts H (2019) Moving forward: on the limits of motor-based forward models. Trends Cogn Sci 23:743–753. https://doi.org/10.1016/j.tics.2019.06.008
Dum RP, Levinthal DJ, Strick PL (2009) The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J Neurosci 29:14223–14235. https://doi.org/10.1523/JNEUROSCI.3398-09.2009
Elsner B, Hommel B (2001) Effect anticipation and action control. J Exp Psychol Hum Percept Perform 27:229–240
Elsner B, Hommel B, Mentschel C, Drzezga A, Prinz W, Conrad B, Siebner H (2002) Linking actions and their perceivable consequences in the human brain. Neuroimage 17:364–372. https://doi.org/10.1006/nimg.2002.1162
Falkenstein M, Hohnsbein J, Hoormann J (1995) Event-related potential correlates of errors in reaction tasks. Electroencephalogr Clin Neurophysiol Suppl 44:287–296
Fan J, Hof P, Guise K, Fossella J, Posner M (2007) The functional integration of the anterior cingulate cortex during conflict processing. Cereb Cortex. https://doi.org/10.1093/cercor/bhm125
Ferrão Y, Pedro A, Hounie A, Mathis M, RosáRio M, Miguel E (2013) The phenomenology of obsessive-compulsive symptoms in Tourette syndrome. In: Martino D, Leckman JF (eds) Tourette syndrome, vol 692. Oxford University Press, New York, pp 50–73
Fiehler K, Ullsperger M, von Cramon DY (2004) Neural correlates of error detection and error correction: is there a common neuroanatomical substrate? Eur J Neurosci 19:3081–3087
Flach R, Press C, Badets A, Heyes C (2010) Shaking hands: priming by social action effects. Br J Psychol 101:739–749. https://doi.org/10.1348/000712609X484595
Flanagan JR, Johansson RS (2003) Action plans used in action observation. Nature 424:769–771. https://doi.org/10.1038/nature01861
Gehring WJ, Coles MG, Meyer DE, Donchin E (1990) The error-related negativity: An event related potential accompanying errors. Psychophysiology 27:S34
Gillan CM, Robbins TW (2014) Goal-directed learning and obsessive-compulsive disorder. Philos Trans R Soc Lond B. https://doi.org/10.1098/rstb.2013.0475
Graybiel AM, Rauch SL (2000) Toward a neurobiology of obsessive-compulsive disorder. Neuron 28:343–347
Greenwald AG (1970) Sensory feedback mechanisms in performance control: with special reference to the ideo-motor mechanism. Psychol Rev 77:73–99
Grèzes J (1998) Top down effect of strategy on the perception of human biological motion: a pet investigation. Cogn Neuropsychol 15:553–582. https://doi.org/10.1080/026432998381023
Hanakawa T, Dimyan MA, Hallett M (2008) Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb Cortex. https://doi.org/10.1093/cercor/bhn036
Heyes C (2001) Causes and consequences of imitation. Trends Cogn Sci 5:253–261
Higuchi S, Holle H, Roberts N, Eickhoff SB, Vogt S (2012) Imitation and observational learning of hand actions: prefrontal involvement and connectivity. Neuroimage 59:1668–1683. https://doi.org/10.1016/j.neuroimage.2011.09.021
Hoffmann S, Falkenstein M (2010) Independent component analysis of erroneous and correct responses suggests online response control. Hum Brain Mapp 31:1305–1315. https://doi.org/10.1002/hbm.20937
Hoffstaedter F, Grefkes C, Caspers S et al (2014) The role of anterior midcingulate cortex in cognitive motor control: evidence from functional connectivity analyses. Hum Brain Mapp 35:2741–2753. https://doi.org/10.1002/hbm.22363
Holroyd CB, Nieuwenhuis S, Yeung N, Nystrom L, Mars RB, Coles MG, Cohen JD (2004) Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nat Neurosci 7:497–498
Hommel B, Müsseler J, Aschersleben G, Prinz W (2001) The theory of event coding (TEC): a framework for perception and action planning. Behav Brain Sci 24:849–878
Hoshi E, Sawamura H, Tanji J (2005) Neurons in the rostral cingulate motor area monitor multiple phases of visuomotor behavior with modest parametric selectivity. J Neurophysiol 94:640–656
Kerns JG, Cohen JD, MacDonald AW 3rd, Cho RY, Stenger VA, Carter CS (2004) Anterior cingulate conflict monitoring and adjustments in control. Science 303:1023–1026
Knoblich G, Prinz W (2005) Linking perception and action: an ideomotor approach. In: Freund H, Jeannerod M, Hallett M, Leiguarda R (eds) Higher-order motor disorders: from neuroanatomy and neurobiology to clinical neurology. Oxford University Press, Oxford, pp 79–104
Koch I, Hoffmann J (2000) The role of stimulus-based and response-based spatial information in sequence learning. J Exp Psychol Learn Mem Cogn 26:863–882. https://doi.org/10.1037//0278-7393.26.4.863
Koch I, Kunde W (2002) Verbal response-effect compatibility. Memory Cognition 30:1297–1303
Kremer S, Chassagnon S, Hoffmann D, Benabid AL, Kahane P (2001) The cingulate hidden hand. J Neurol Neurosurg Psychiatry 70:264–265. https://doi.org/10.1136/jnnp.70.2.264
Kunde W (2001) Response-effect compatibility in manual choice reaction tasks. J Exp Psychol Hum Percept Perform 27:387–394. https://doi.org/10.1037//OO96-1523.27.2.387
Kunde W (2004) Response priming by supraliminal and subliminal action effects. Psychol Res 68:91–96. https://doi.org/10.1007/s00426-003-0147-4
Kunde W, Koch I, Hoffmann J (2004) Anticipated action effects affect the selection, initiation, and execution of actions. Q J Exp Psychol Sec A 57:87–106. https://doi.org/10.1080/02724980343000143
Kunde W, Schmidts C, Wirth R, Herbort O (2017) Action effects are coded as transitions from current to future stimulation: Evidence from compatibility effects in tracking. J Exp Psychol Hum Percept Perform 43:477–486. https://doi.org/10.1037/xhp0000311
Lancaster JL, Tordesillas-Gutiérrez D, Martinez M et al (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28:1194–1205. https://doi.org/10.1002/hbm.20345
Maltby N, Tolin DF, Worhunsky P, O’Keefe TM, Kiehl KA (2005) Dysfunctional action monitoring hyperactivates frontal-striatal circuits in obsessive-compulsive disorder: an event-related fMRI study. Neuroimage 24:495–503
Mataix-Cols D, Wooderson S, Lawrence N, Brammer MJ, Speckens A, Phillips ML (2004) Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Arch Gen Psychiatry 61:564–576
Mayr U (2004) Conflict, consciousness, and control. Trends Cogn Sci 8:145–148. https://doi.org/10.1016/j.tics.2004.02.006
Melcher T, Weidema M, Eenshuistra RM, Hommel B, Gruber O (2008) The neural substrate of the ideomotor principle: an event-related fMRI analysis. Neuroimage 39:1274–1288. https://doi.org/10.1016/j.neuroimage.2007.09.049
Melcher T, Winter D, Hommel B, Pfister R, Dechent P, Gruber O (2013) The neural substrate of the ideomotor principle revisited: evidence for asymmetries in action-effect learning. Neuroscience 231:13–27. https://doi.org/10.1016/j.neuroscience.2012.11.035
Michelet T, Bioulac B, Guehl D, Escola L, Burbaud P (2007) Impact of commitment on performance evaluation in the rostral cingulate motor area. J Neurosci 27:7482–7489
Michelet T, Bioulac B, Guehl D, Goillandeau M, Burbaud P (2009) Single medial prefrontal neurons cope with error. PLoS ONE 4:e6240. https://doi.org/10.1371/journal.pone.0006240
Michelet T, Bioulac B, Langbour N, Goillandeau M, Guehl D, Burbaud P (2016) Electrophysiological correlates of a versatile executive control system in the monkey anterior cingulate cortex. Cereb Cortex 26:1684–1697. https://doi.org/10.1093/cercor/bhv004
Miltner W, Braun C, Coles MG (1997) Event-related brain potentials following incorrect feedback in a time-estimation task: evidence for a “generic” neural system for error detection. J Cogn Neurosci 9:788–798
Moschl M, Fischer R, Bugg JM, Scullin MK, Goschke T, Walser M (2020) Aftereffects and deactivation of completed prospective memory intentions: a systematic review. Psychol Bull 146:245–278. https://doi.org/10.1037/bul0000221
Nattkemper D, Ziessler M (2004) Cognitive control of action: the role of action effects. Psychol Res 68:71–73. https://doi.org/10.1007/s00426-003-0145-6
Nieuwenhuis S, Ridderinkhof KR, Blom J, Band GP, Kok A (2001) Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. Psychophysiology 38:752–760
Oliveira FTP, McDonald JJ, Goodman D (2007) Performance monitoring in the anterior cingulate is not all error related: expectancy deviation and the representation of action-outcome associations. J Cogn Neurosci 19:1994–2004. https://doi.org/10.1162/jocn.2007.19.12.1994
Osiurak F, Badets A (2016) Tool use and affordance: manipulation-based versus reasoning-based approaches. Psychol Rev 123:534–568. https://doi.org/10.1037/rev0000027
Parvizi J, Rangarajan V, Shirer WR, Desai N, Greicius MD (2013) The will to persevere induced by electrical stimulation of the human cingulate gyrus. Neuron 80:1359–1367. https://doi.org/10.1016/j.neuron.2013.10.057
Pfister R (2019) Effect-based action control with body-related effects: implications for empirical approaches to ideomotor action control. Psychol Rev 126:153–161. https://doi.org/10.1037/rev0000140
Pfister R, Melcher T, Kiesel A, Dechent P, Gruber O (2014) Neural correlates of ideomotor effect anticipations. Neuroscience 259:164–171. https://doi.org/10.1016/j.neuroscience.2013.11.061
Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342–353
Prado HS, Rosário MC, Lee J, Hounie AG, Shavitt RG, Miguel EC (2008) Sensory phenomena in obsessive-compulsive disorder and tic disorders: a review of the literature. CNS Spectr 13:425–432. https://doi.org/10.1017/s1092852900016606
Prinz W (1997) Perception and action planning. Eur J Cogn Psychol 2:1–26
Procyk E, Wilson CRE, Stoll FM, Faraut MCM, Petrides M, Amiez C (2014) Midcingulate motor map and feedback detection: converging data from humans and monkeys. Cereb Cortex. https://doi.org/10.1093/cercor/bhu213
Rabbitt PM (1966) Errors and error correction in choice-response tasks. J Exp Psychol 71:264–272
Rabbitt P, Rodgers B (1977) What does a man do after he makes an error? An analysis of response programming. Q J Exp Psychol 29:727–743. https://doi.org/10.1080/14640747708400645
Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192. https://doi.org/10.1146/annurev.neuro.27.070203.144230
Rizzolatti G, Fabbri-Destro M, Cattaneo L (2009) Mirror neurons and their clinical relevance. Nat Clin Pract Neurol 5:24–34. https://doi.org/10.1038/ncpneuro0990
Roger C, Bénar CG, Vidal F, Hasbroucq T, Burle B (2010) Rostral cingulate zone and correct response monitoring: ICA and source localization evidences for the unicity of correct- and error-negativities. Neuroimage 51:391–403. https://doi.org/10.1016/j.neuroimage.2010.02.005
Rotgé J-Y, Langbour N, Dilharreguy B et al (2015) Contextual and behavioral influences on uncertainty in obsessive-compulsive disorder. Cortex 62:1–10. https://doi.org/10.1016/j.cortex.2012.12.010
Rounis E, Banca P, Voon V (2016) Deficits in limb praxis in patients with obsessive-compulsive disorder. J Neuropsychiatry Clin Neurosci 28:232–235. https://doi.org/10.1176/appi.neuropsych.15090233
Rushworth MF, Hadland KA, Paus T, Sipila PK (2002) Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. J Neurophysiol 87:2577–2592
Schuch S, Tipper SP (2007) On observing another person’s actions: influences of observed inhibition and errors. Percept Psychophys 69:828–837
Schwartz JM (1999) A role for volition and attention in the generation of new brain circuitry. Toward a nerobiology of mental force. J Conscious Stud 6:115–142
Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ (2011) The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 12:154–167. https://doi.org/10.1038/nrn2994
Shin YK, Proctor RW, Capaldi EJ (2010) A review of contemporary ideomotor theory. Psychol Bull 136:943–974. https://doi.org/10.1037/a0020541
Swick D, Turken AU (2002) Dissociation between conflict detection and error monitoring in the human anterior cingulate cortex. Proc Natl Acad Sci 99:16354–16359
Talairach J, Bancaud J, Geier S, Bordas-Ferrer M, Bonis A, Szikla G, Rusu M (1973) The cingulate gyrus and human behaviour. Electroencephalogr Clin Neurophysiol 34:45–52
Ullsperger M, Danielmeier C, Jocham G (2014) Neurophysiology of performance monitoring and adaptive behavior. Physiol Rev 94:35–79
Van Schie HT, Mars RB, Coles MG, Bekkering H (2004) Modulation of activity in medial frontal and motor cortices during error observation. Nat Neurosci 7:549–554
Vogt BA (2009) Regions and subregions of the cingulate cortex. In: Vogt BA (ed) Cingulate neurobiology and disease. Oxford University Press, London, pp 3–30
Vogt BA (2016) Midcingulate cortex: Structure, connections, homologies, functions and diseases. J Chem Neuroanat 74:28–46. https://doi.org/10.1016/j.jchemneu.2016.01.010
Vogt BA, Devinsky O (2000) Topography and relationships of mind and brain. Prog Brain Res 122:11–22. https://doi.org/10.1016/S0079-6123(08)62127-5
Walton ME, Devlin JT, Rushworth MFS (2004) Interactions between decision making and performance monitoring within prefrontal cortex. Nat Neurosci 7:1259–1265. https://doi.org/10.1038/nn1339
Weller L, Schwarz KA, Kunde W, Pfister R (2018) My mistake? Enhanced error processing for commanded compared to passively observed actions. Psychophysiology. https://doi.org/10.1111/psyp.13057
Williams ZM, Bush G, Rauch SL, Cosgrove GR, Eskandar EN (2004) Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nat Neurosci 7:1370–1375
Wolpert DM, Ghahramani Z, Flanagan JR (2001) Perspectives and problems in motor learning. Trends Cogn Sci 5:487–494
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Michelet, T., Badets, A. The anterior midcingulate cortex might be a neuronal substrate for the ideomotor mechanism. Exp Brain Res 239, 2345–2355 (2021). https://doi.org/10.1007/s00221-021-06159-9
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DOI: https://doi.org/10.1007/s00221-021-06159-9