Brain Topography

, Volume 29, Issue 5, pp 679–692 | Cite as

Brain Activation Patterns Characterizing Different Phases of Motor Action: Execution, Choice and Ideation

  • Simona Gardini
  • Annalena Venneri
  • William Jonathan McGeown
  • Cristian Toraci
  • Luca Nocetti
  • Carlo Adolfo Porro
  • Paolo Caffarra
Original Paper


Motor behaviour is controlled by a large set of interacting neural structures, subserving the different components involved in hierarchical motor processes. Few studies have investigated the neural substrate of higher-order motor ideation, i.e. the mental operation of conceiving a movement. The aim of this functional magnetic resonance imaging study was to segregate the neural structures involved in motor ideation from those involved in movement choice and execution. An index finger movement paradigm was adopted, including three different conditions: performing a pre-specified movement, choosing and executing a movement and ideating a movement of choice. The tasks involved either the right or left hand, in separate runs. Neuroimaging results were obtained by comparing the different experimental conditions and computing conjunction maps of the right and left hands for each contrast. Pre-specified movement execution was supported by bilateral fronto-parietal motor regions, the cerebellum and putamen. Choosing and executing finger movement involved mainly left fronto-temporal areas and the anterior cingulate. Motor ideation activated almost exclusively left hemisphere regions, including the inferior, middle and superior frontal regions, middle temporal and middle occipital gyri. These findings show that motor ideation is controlled by a cortical network mainly involved in abstract thinking, cognitive and motor control, semantic and visual imagery processes.


Movement Ideation Motor ideation fMRI Finger movement 



This study was supported by funding from Fondazione Cassa di Risparmio of Parma and Piacenza and ex 60 % F.I.L. to P.C. and by a grant from MIUR (Italy) to A.V.

Compliance with Ethical Standards

Conflict of interest

All authors declare that they have no conflict of interest.


  1. Bajaj S, Butler AJ, Drake D, Dhamala M (2015) Brain effective connectivity during motor-imagery and execution following stroke and rehabilitation. Neuroimage 8:572–582CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bernstein NA (1996) On dexterity and its development. In: Latash ML, Turvey MT (eds) Dexterity and its development. Lawrence Erlbaum Associates, MahwahGoogle Scholar
  3. Bolognini N, Convento S, Banco E, Mattioli F, Tesio L, Vallar G (2015) Improving ideomotor limb apraxia by electrical stimulation of the left posterior parietal cortex. Brain 138:428–439CrossRefPubMedGoogle Scholar
  4. Borra E, Belmalih A, Calzavara R, Gerbella M, Murata A, Rozzi S, Luppino G (2008) Cortical connections of the macaque anterior intraparietal (AIP) area. Cereb Cortex 18:1094–1111CrossRefPubMedGoogle Scholar
  5. Breveglieri R, Galletti C, Dal Bò G, Hadjidimitrakis K, Fattori P (2014) Multiple aspects of neural activity during reaching preparation in the medial posterior parietal area V6A. J Cogn Neurosci 26:878–895CrossRefPubMedGoogle Scholar
  6. Coubard OA, Urbanski M, Bourlon C, Gaumet M (2014) Educating the blind brain: a panorama of neural bases of vision and of training programs in organic neurovisual deficits. Front Integr Neurosci 8:89CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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 15:373–385CrossRefPubMedGoogle Scholar
  8. De Renzi E, Lucchelli F (1988) Ideational apraxia. Brain 111:1173–1185CrossRefPubMedGoogle Scholar
  9. Drew T, Marigold DS (2015) Taking the next step: cortical contributions to the control of locomotion. Curr Opin Neurobiol 33:25–33CrossRefPubMedGoogle Scholar
  10. Dum RP, Strick PL (2002) Motor areas in the frontal lobe of the primate. Physiol Behav 77:677–682CrossRefPubMedGoogle Scholar
  11. Fried I, Mukamel R, Kreiman G (2011) Internally generated preactivation of single neurons in human medial frontal cortex predicts volition. Neuron 69:548–562CrossRefPubMedPubMedCentralGoogle Scholar
  12. Friston KJ, Holmes AP, Price CJ, Büchel C, Worsley KJ (1999) Multisubject fMRI studies and conjunction analyses. Neuroimage 10:385–396CrossRefPubMedGoogle Scholar
  13. Frith C (1991) Positron emission tomography studies of the frontal lobe function relevance to psychiatric disease. Ciba Found Symp 163:181–191PubMedGoogle Scholar
  14. Gao Q, Duan X, Chen H (2011) Evaluation of effective connectivity of motor areas during motor imagery and execution using conditional Granger causality. Neuroimage 54:1280–1288CrossRefPubMedGoogle Scholar
  15. Gardini S, De Beni R, Cornoldi C, Bromiley A, Venneri A (2005) Different neuronal pathways support the generation of general and specific mental images. Neuroimage 27:544–552CrossRefPubMedGoogle Scholar
  16. Gardini S, Cornoldi C, De Beni R, Venneri A (2006) Left mediotemporal structures mediate the retrieval of episodic autobiographical mental images. Neuroimage 30:645–655CrossRefPubMedGoogle Scholar
  17. Gardini S, Concari L, Pagliara S, Ghetti C, Venneri A, Caffarra P (2011) Visuo-spatial imagery impairment in posterior cortical atrophy: a cognitive and SPECT study. Behav Neurol 24:123–132CrossRefPubMedGoogle Scholar
  18. Grafton ST, Hamilton AF (2007) Evidence for a distributed hierarchy of action representation in the brain. Hum Mov Sci 26:590–616CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gross RG, Grossman M (2008) Update on apraxia. Curr Neurol Neurosci Rep 8:490–496CrossRefPubMedGoogle Scholar
  20. Hanakawa T (2011) Rostral premotor cortex as a gateway between motor and cognitive networks. Neurosci Res 70:144–154CrossRefPubMedGoogle Scholar
  21. Hécaen H (1972) Introduction à la neuro-psychologie. Librairie Larousse, ParisGoogle Scholar
  22. Huey ED, Pardini M, Cavanagh A, Wassermann EM, Kapogiannis D, Spina S, Ghetti B, Grafman J (2009) Association of ideomotor apraxia with frontal gray matter volume loss in corticobasal syndrome. Arch Neurol 66:1274–1280CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ingvar DH, Philipson L (1977) Distribution of cerebral blood flow in the dominant hemisphere during motor ideation and motor performance. Ann Neurol 3:230–237CrossRefGoogle Scholar
  24. Koch G, Rothwell JC (2009) TMS investigations into the task-dependent functional interplay between human posterior parietal and motor cortex. Behav Brain Res 202:147–152CrossRefPubMedGoogle Scholar
  25. Lui F, Buccino G, Duzzi D, Benuzzi F, Crisi G, Baraldi P, Nichelli P, Porro CA, Rizzolatti G (2008) Neural substrates for observing and imagining non object-directed actions. Soc Neurosci 3:261–275CrossRefPubMedGoogle Scholar
  26. Mammarella N, Cornoldi C, Pazzaglia F (2004) Psicologia dell’apprendimento multimediale. Il Mulino, BolognaGoogle Scholar
  27. Manuel AL, Radman N, Mesot D, Chouiter L, Clarke S, Annoni JM, Spierer L (2013) Inter- and intrahemispheric dissociations in ideomotor apraxia: a large-scale lesion-symptom mapping study in subacute brain-damaged patients. Cereb Cortex 23:2781–2789CrossRefPubMedGoogle Scholar
  28. Matelli M, Luppino G (2001) Parietofrontal circuits for action and space perception in the macaque monkey. Neuroimage 14:S27–S32CrossRefPubMedGoogle Scholar
  29. Matsuda I, Nittono H (2015) The intention to conceal activates the right prefrontal cortex: an event-related potential study. NeuroReport 26:223–227CrossRefPubMedGoogle Scholar
  30. Matsumoto R, Nair DR, Ikeda A, Fumuro T, Lapresto E, Mikuni N, Bingaman W, Miyamoto S, Fukuyama H, Takahashi R, Najm I, Shibasaki H, Lüders HO (2012) Parieto-frontal network in humans studied by cortico-cortical evoked potential. Hum Brain Mapp 33:2856–2872CrossRefPubMedGoogle Scholar
  31. Morawetz C, Bode S, Baudewig J, Kirilina E, Heekeren HR (2015) Changes in effective connectivity between dorsal and ventral prefrontal regions moderate emotion regulation. Cereb Cortex. doi: 10.1093/cercor/bhv005
  32. Olsson CJ, Nyberg L (2010) Motor imagery: if you can’t do it, you won’t think it. Scand J Med Sci Sports 20:711–715CrossRefPubMedGoogle Scholar
  33. Paivio A (1971) Imagery and verbal processes. Holt, Rinehart, and Winston, New YorkGoogle Scholar
  34. Pellegrino G, Làdavas E (2015) Peripersonal space in the brain. Neuropsychologia 66C:126–133CrossRefGoogle Scholar
  35. Raffin E, Mattout J, Reilly KT, Giraux P (2012) Disentangling motor execution from motor imagery with the phantom limb. Brain 135:582–595CrossRefPubMedGoogle Scholar
  36. Rao SM, Binder JR, Bandettini BS, Hammeke TA, Yetkin FZ, Jesmanowicz A, Lisk LM, Morris GL, Mueller WM, Estkowski LD et al (1993) Functional magnetic resonance imaging of complex human movements. Neurology 43:2311–2318CrossRefPubMedGoogle Scholar
  37. Rizzolatti G, Fogassi L (2014) The mirror mechanism: recent findings and perspectives. Philos Trans R Soc B 369:20130420CrossRefGoogle Scholar
  38. Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31:889–901CrossRefPubMedGoogle Scholar
  39. Schluter ND, Krams M, Rushworth MFS, Passingham RE (2001) Cerebral dominance for action in the human brain: the selection of actions. Neuropsychologia 39:105–113CrossRefPubMedGoogle Scholar
  40. Schulz KP, Bédard AC, Czarnecki R, Fan J (2011) Preparatory activity and connectivity in dorsal anterior cingulate cortex for cognitive control. Neuroimage 57:242–250CrossRefPubMedPubMedCentralGoogle Scholar
  41. Shamay-Tsoory SG, Adler N, Aharon-Peretz J, Perry D, Mayseless N (2011) The origins of originality: the neural bases of creative thinking and originality. Neuropsychologia 49:178–185CrossRefPubMedGoogle Scholar
  42. Sharma N, Pomeroy VM, Baron JC (2006) Motor imagery: a backdoor to the motor system after stroke? Stroke 37:1941–1952CrossRefPubMedGoogle Scholar
  43. Simmons WK, Martin A (2009) The anterior temporal lobes and the functional architecture of semantic memory. J Int Neuropsychol Soc 15:645–649CrossRefPubMedPubMedCentralGoogle Scholar
  44. Singer JL, Antrobus JS (1972) Daydreamer, imaginal processes, and personality: a normative study. In: Sheehan PW (ed) The function and nature of imagery. Academic Press, New York, pp 175–202Google Scholar
  45. Tabibnia G, Creswell JD, Kraynak T, Westbrook C, Julson E, Tindle HA (2014) Common prefrontal regions activate during self-control of craving, emotion, and motor impulses in smokers. Clin Psychol Sci 2:611–619CrossRefPubMedPubMedCentralGoogle Scholar
  46. Tanji J, Hoshi E (2008) Role of the lateral prefrontal cortex in executive behavioral control. Physiol Rev 88:37–57CrossRefPubMedGoogle Scholar
  47. Toma K, Nakai T (2002) Functional MRI in human control studies and clinical applications. Magn Reson Med Sci 1:109–120CrossRefPubMedGoogle Scholar
  48. Tomasino B, Rumiati RI, Umiltà CA (2003) Selective deficit of motor imagery as tapped by a left-right decision of visually presented hands. Brain Cogn 53:376–380CrossRefPubMedGoogle Scholar
  49. Waldvogel D, van Gelderen P, Ishii K, Hallett M (1999) The effect of movement amplitude on activation in functional magnetic resonance imaging studies. J Cereb Blood Flow Metab 19:1209–1212CrossRefPubMedGoogle Scholar
  50. Zimmer HD (2008) Visual and spatial working memory: from boxes to networks. Neurosci Biobehav Rev 32:1373–1395CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Simona Gardini
    • 1
  • Annalena Venneri
    • 2
    • 3
  • William Jonathan McGeown
    • 4
  • Cristian Toraci
    • 5
  • Luca Nocetti
    • 6
  • Carlo Adolfo Porro
    • 7
  • Paolo Caffarra
    • 1
    • 8
  1. 1.Department of NeuroscienceUniversity of ParmaParmaItaly
  2. 2.Department of NeuroscienceUniversity of SheffieldSheffieldUK
  3. 3.IRCCS, Fondazione Ospedale S. CamilloVeniceItaly
  4. 4.School of Psychological Sciences and HealthUniversity of StrathclydeGlasgowUK
  5. 5.Biolab, Department of CommunicationUniversity of GenoaGenoaItaly
  6. 6.Struttura Complessa di Fisica SanitariaAzienda Ospedaliero-Universitaria di Modena e Reggio EmiliaModenaItaly
  7. 7.Department of Biomedical, Metabolic and Neural Sciences, Section of Human PhysiologyUniversity of Modena and Reggio EmiliaModenaItaly
  8. 8.Centre for Cognitive Disorders and Dementia (CDCD)AUSLParmaItaly

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