Brain Imaging and Behavior

, Volume 12, Issue 4, pp 919–930 | Cite as

Illusory limb movements activate different brain networks than imposed limb movements: an ALE meta-analysis

  • Jeffrey M. Kenzie
  • Ettie Ben-Shabat
  • Gemma Lamp
  • Sean P. Dukelow
  • Leeanne M. Carey
Original Research


Proprioceptive information allows us to perform smooth coordinated movements by constantly updating us with knowledge of the position of our limbs in space. How this information is combined and processed to form conscious perceptions of limb position is still relatively unknown. Several functional neuroimaging studies have attempted to tease out the brain areas responsible for proprioceptive processing in the human brain. Yet there still exists some disagreement in the specific brain regions involved. In order to consolidate the current knowledge in the field, we performed a systematic review of the literature and an activation likelihood estimation (ALE) meta-analysis of functional neuroimaging studies of proprioception. We identified 12 studies that used a proprioceptive stimulus of the upper extremity for ALE analysis (n = 141 participants). Two types of stimuli (illusion of movement induced through muscle tendon vibration and passive/imposed movements) were found to be most commonly used to probe proprioceptive networks in the brain. ALE analysis of these two stimulus types revealed that both were associated with activation in the left precentral, postcentral, and anterior cingulate gyri. Interestingly, different patterns of activation were also observed between illusions of movement and imposed movement. In the left hemisphere, imposed movements resulted in activations that were more inferior in the post-central gyrus. In the right hemisphere, imposed movements resulted in two clusters of activation in the inferior aspect of the precentral gyrus and the hand area of the post-central gyrus, while illusions of movement resulted in a single cluster of activation in the inferior parietal lobule. These results suggest that illusions of movement without limb displacement may activate different brain areas compared with actual limb displacement. Careful consideration should be made in future studies when selecting a proprioceptive stimulus to probe these brain networks.


Proprioception Activation likelihood estimation Meta-analysis Neuroimage fMRI Position sense Kinesthesis 



This work was supported by the RHISE HBI-Melbourne Trainee Exchange Program (awarded to JMK and supervised by LMC; the program is co-supported by Rebecca Hotchkiss International Scholar Exchange and Hotchkiss Brain Institute, Calgary, and the University of Melbourne and Florey Institute of Neuroscience and Mental Health, Melbourne). JMK was supported by an Alberta-Innovates Health-Solutions MD/PhD studentship. The work was also supported by NHMRC project grant (APP1022684 to LMC); James S. McDonnell Foundation Collaborative Award (#220020413 to LMC); NHMRC Centre of Research Excellence in Stroke Rehabilitation and Brain Injury (#1077898 to LMC); Victorian Government’s Operational Infrastructure Support Program; an Australian Research Council Future Fellowship awarded to LMC [#FT0992299].

Compliance with ethical standards


This work was supported by a RHISE HBI-Melbourne Trainee Exchange Program (awarded to JMK and supervised by LMC; the program is co-supported by Rebecca Hotchkiss International Scholar Exchange and Hotchkiss Brain Institute, Calgary, and the University of Melbourne and Florey Institute of Neuroscience and Mental Health, Melbourne). JMK was supported by an Alberta-Innovates Health-Solutions MD/PhD studentship. The work was also supported by NHMRC project grant (APP1022684 to LMC); James S. McDonnell Foundation Collaborative Award (#220020413 to LMC); NHMRC Centre of Research Excellence in Stroke Rehabilitation and Brain Injury (#1077898 to LMC); Victorian Government’s Operational Infrastructure Support Program; an Australian Research Council Future Fellowship awarded to LMC [#FT0992299].

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article contains data from previously published studies and does not contain any new data from human participants or animals performed by any of the authors.

Supplementary material

11682_2017_9756_MOESM1_ESM.docx (52 kb)
Supplementary Table 1 (DOCX 52 kb)


  1. Bauer, C. C. C., Díaz, J.-L., Concha, L., & Barrios, F. A. (2014). Sustained attention to spontaneous thumb sensations activates brain somatosensory and other proprioceptive areas. Brain and Cognition, 87(April), 86–96. doi: 10.1016/j.bandc.2014.03.009.CrossRefPubMedGoogle Scholar
  2. Ben-Shabat, E., Matyas, T. A., Pell, G. S., Brodtmann, A., & Carey, L. M. (2015). The right Supramarginal Gyrus is important for proprioception in healthy and stroke-affected participants: a functional MRI study. Frontiers in Neurology, 6, 248. doi: 10.3389/fneur.2015.00248.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bowsher, B. D., & Systems, T. (1965). The anatomophysiological basis of somatosensory discrimination. International Review of Neurobiology, 8, 35–75.CrossRefPubMedGoogle Scholar
  4. Carey, L. M., & Matyas, T. A. (2011). Frequency of discriminative sensory loss in the hand after stroke in a rehabilitation setting. Journal of Rehabilitation Medicine, 43, 257–263.CrossRefPubMedGoogle Scholar
  5. Carey, L. M., Oke, L. E., & Matyas, T. A. (1996). Impaired limb position sense after stroke: a quantitative test for clinical use. Archives of Physical Medicine and Rehabilitation, 77(12), 1271–1278 Retrieved from Scholar
  6. Christensen, M. S., & Grey, M. J. (2013). Modulation of proprioceptive feedback during functional electrical stimulation: an fMRI study. European Journal of Neuroscience, 37(11), 1766–1778. doi: 10.1111/ejn.12178.CrossRefPubMedGoogle Scholar
  7. Cignetti, F., Vaugoyeau, M., Nazarian, B., Roth, M., Anton, J.-L., & Assaiante, C. (2014). Boosted activation of right inferior frontoparietal network: a basis for illusory movement awareness. Human Brain Mapping, 35(10), 5166–5178. doi: 10.1002/hbm.22541.CrossRefPubMedGoogle Scholar
  8. Dukelow, S. P., Herter, T. M., Moore, K. D., Demers, M. J., Glasgow, J. I., Bagg, S. D., et al. (2010). Quantitative assessment of limb position sense following stroke. Neurorehabilitation and Neural Repair, 24(2), 178–187. doi: 10.1177/1545968309345267.CrossRefPubMedGoogle Scholar
  9. Edin, B. B., & Abbs, J. H. (1991). Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. Journal of Neurophysiology, 65(3), 657–670 Retrieved from Scholar
  10. Eickhoff, S. B., Laird, A. R., Grefkes, C., Wang, L. E., Zilles, K., & Fox, P. T. (2009). Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data : a random-effects approach based on empirical estimates of spatial uncertainty. Human Brain Mapping, 30(November 2008), 2907–2926. doi: 10.1002/hbm.20718.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Eickhoff, S. B., Bzdok, D., Laird, A. R., Roski, C., Zilles, K., & Fox, P. T. (2011). Co-activation patterns distinguish cortical modules, their connectivity and functional differentiation. NeuroImage, 57(3), 938–949. doi: 10.1016/j.neuroimage.2011.05.021.Co-activation.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Eickhoff, S. B., Bzdok, D., Laird, A. R., Kurth, F., & Fox, P. T. (2012). Activation likelihood estimation meta-analysis revisited. NeuroImage, 59(3), 2349–2361. doi: 10.1016/j.neuroimage.2011.09.017.CrossRefPubMedGoogle Scholar
  13. Eickhoff, S. B., Laird, A. R., Fox, P. M., Lancaster, J. L., & Fox, P. T. (2017). Implementation errors in the GingerALE software: description and recommendations. Human Brain Mapping, 38(1), 7–11. doi: 10.1002/hbm.23342.CrossRefPubMedGoogle Scholar
  14. Findlater, S. E., Desai, J. A., Semrau, J. A., Kenzie, J. M., Rorden, C., Herter, T. M., et al. (2016). Central perception of position sense involves a distributed neural network – Evidence from lesion-behaviour analyses. Cortex, 79, 42–56. doi: 10.1016/j.cortex.2016.03.008.CrossRefPubMedGoogle Scholar
  15. Gardner, E., & Johnson, K. (2013). Touch. In Principles of Neural Science (5th edn, pp. 498–526). McGraw-Hill Medical.Google Scholar
  16. Goble, D. J., Coxon, J. P., Van Impe, A., Geurts, M., Van Hecke, W., Sunaert, S., et al. (2012). The neural basis of central proprioceptive processing in older versus younger adults: an important sensory role for right putamen. Human Brain Mapping, 33(4), 895–908. doi: 10.1002/hbm.21257.CrossRefPubMedGoogle Scholar
  17. Goodwin, G. M., McCloskey, D. I., & Matthews, P. B. (1972a). Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science (New York, N.Y.), 175(4028), 1382–1384 Retrieved from Scholar
  18. Goodwin, G. M., Mccloskey, D. I., & Matthews, P. B. C. (1972b). The contribution of muscle afferents to kinesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain, 95, 705–748.CrossRefPubMedGoogle Scholar
  19. Habas, C., & Cabanis, E. A. (2007). The neural network involved in a bimanual tactile-tactile matching discrimination task: a functional imaging study at 3 T. Neuroradiology, 49(8), 681–688. doi: 10.1007/s00234-007-0239-8.CrossRefPubMedGoogle Scholar
  20. Hagura, N., Takei, T., Hirose, S., Aramaki, Y., Matsumura, M., Sadato, N., & Naito, E. (2007). Activity in the posterior parietal cortex mediates visual dominance over kinesthesia. The Journal of Neuroscience, 27(26), 7047–7053. doi: 10.1523/JNEUROSCI.0970-07.2007.CrossRefPubMedGoogle Scholar
  21. Hagura, N., Oouchida, Y., Aramaki, Y., Okada, T., Matsumura, M., Sadato, N., & Naito, E. (2009). Visuokinesthetic perception of hand movement is mediated by cerebro-cerebellar interaction between the left cerebellum and right parietal cortex. Cerebral Cortex, 19(1), 176–186. doi: 10.1093/cercor/bhn068.CrossRefPubMedGoogle Scholar
  22. Kavounoudias, A., Roll, J. P., Anton, J. L., Nazarian, B., Roth, M., & Roll, R. (2008). Proprio-tactile integration for kinesthetic perception: an fMRI study. Neuropsychologia, 46(2), 567–575. doi: 10.1016/j.neuropsychologia.2007.10.002.CrossRefPubMedGoogle Scholar
  23. Kenzie, J. M., Semrau, J. A., Findlater, S. E., Herter, T. M., Hill, M. D., Scott, S. H., & Dukelow, S. P. (2014). Anatomical correlates of proprioceptive impairments following acute stroke: a case series. Journal of the Neurological Sciences, 342(1–2), 52–61. doi: 10.1016/j.jns.2014.04.025.CrossRefPubMedGoogle Scholar
  24. Kenzie, J. M., Semrau, J. A., Findlater, S. E., Yu, A. Y., Jamsheed, A., Herter, T. M., et al. (2016). Localization of impaired kinesthetic processing post-stroke. Frontiers in Human Neuroscience. doi: 10.3389/fnhum.2016.00505.
  25. Kim, J. S. (1992). Pure sensory stroke. Clinical-radiological correlates of 21 cases. Stroke; a Journal of Cerebral Circulation, 23(7), 983–987. doi: 10.1161/01.STR.23.7.983.CrossRefGoogle Scholar
  26. Laird, A. R., Fox, P. M., Price, C. J., Glahn, D. C., Uecker, A. M., Lancaster, J. L., et al. (2005). ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Human Brain Mapping, 25(1), 155–164. doi: 10.1002/hbm.20136.CrossRefPubMedGoogle Scholar
  27. Lancaster, J. L., Tordesillas-Gutierrez, D., Martinez, M., Salinas, F., Evans, A., Zilles, K., et al. (2007). Bias between MNI and talairach coordinates analyzed using the ICBM-152 brain template. Human Brain Mapping, 28(11), 1194–1205. doi: 10.1002/hbm.20345.CrossRefPubMedGoogle Scholar
  28. Loubinoux, I., Tombari, D., Pariente, J., Gerdelat-Mas, A., Franceries, X., Cassol, E., et al. (2005). Modulation of behavior and cortical motor activity in healthy subjects by a chronic administration of a serotonin enhancer. NeuroImage, 27(2), 299–313. doi: 10.1016/j.neuroimage.2004.12.023.CrossRefPubMedGoogle Scholar
  29. Manivannan, M., & Suresh, P. K. (2012). On the somatosensation of vision. Annals of Neurosciences, 19(1), 31–39. doi: 10.5214/ans.0972.7531.180409.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Mccloskey, D. I. (1973). Differences between the senses of movement and position shown by the effects of loading and vibration of muscles in man. Brain Research, 63, 119–131.CrossRefGoogle Scholar
  31. Meyer, S., Kessner, S. S., Cheng, B., Bonstrup, M., Schulz, R., Hummel, F. C., et al. (2016). Voxel-based lesion-symptom mapping of stroke lesions underlying somatosensory deficits. NeuroImage: Clinical, 10, 257–266. doi: 10.1016/j.nicl.2015.12.005.CrossRefGoogle Scholar
  32. Mima, T., Sadato, N., Yazawa, S., Hanakawa, T., Fukuyama, H., Yonekura, Y., & Shibasaki, H. (1999). Brain structures related to active and passive finger movements in man. Brain, 122(1), 1989–1997. doi: 10.1093/brain/122.10.1989.CrossRefPubMedGoogle Scholar
  33. Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Group, T. P. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine, 6(7), e10000097. doi: 10.1371/journal.pmed.1000097.CrossRefGoogle Scholar
  34. Naito, E., & Ehrsson, H. H. (2001). Kinesthetic illusion of wrist movement activates motor-related areas. Neuroreport, 12(17), 3805–3809. doi: 10.1097/00001756-200112040-00041.CrossRefPubMedGoogle Scholar
  35. Naito, E., Ehrsson, H. H., Geyer, S., Zilles, K., & Roland, P. E. (1999). Illusory arm movements activate cortical motor areas: a positron emission tomography study. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 19(14), 6134–6144 Retrieved from Scholar
  36. Naito, E., Roland, P. E., & Ehrsson, H. H. (2002). I feel my hand moving: a new role of the primary motor cortex in somatic perception of limb movement. Neuron, 36(5), 979–988. doi: 10.1016/s0896-6273(02)00980-7.CrossRefPubMedGoogle Scholar
  37. Naito, E., Roland, P. E., Grefkes, C., Choi, H. J., Eickhoff, S., Geyer, S., et al. (2005). Dominance of the right hemisphere and role of area 2 in human kinesthesia. Journal of Neurophysiology, 93(2), 1020–1034. doi: 10.1152/jn.00637.2004.CrossRefPubMedGoogle Scholar
  38. Naito, E., Nakashima, T., Kito, T., Aramaki, Y., Okada, T., & Sadato, N. (2007). Human limb-specific and non-limb-specific brain representations during kinesthetic illusory movements of the upper and lower extremities. The European Journal of Neuroscience, 25(11), 3476–3487. doi: 10.1111/j.1460-9568.2007.05587.x.CrossRefPubMedGoogle Scholar
  39. Penfield, W. (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 60(4), 389–443. doi: 10.1093/brain/60.4.389.CrossRefGoogle Scholar
  40. Radovanovic, S., Korotkov, A., Ljubisavljevic, M., Lyskov, E., Thunberg, J., Kataeva, G., et al. (2002). Comparison of brain activity during different types of proprioceptive inputs: a positron emission tomography study. Experimental Brain Research, 143(3), 276–285. doi: 10.1007/s00221-001-0994-4.CrossRefPubMedGoogle Scholar
  41. Roll, J. P., & Vedel, J. P. (1982). Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Experimental Brain Research, 47, 177–190.CrossRefPubMedGoogle Scholar
  42. Romaiguere, P., Anton, J., Roth, M., Casini, L., & Roll, J. (2003). Motor and parietal cortical areas both underlie kinaesthesia. Cognitive Brain Research, 16(1), 74–82. doi: 10.1016/s0926-6410(02)00221-5.CrossRefPubMedGoogle Scholar
  43. Rorden, C., Karnath, H.-O., & Bonilha, L. (2007). Improving lesion-symptom mapping. Journal of Cognitive Neuroscience, 19(7), 1081–1088. doi: 10.1162/jocn.2007.19.7.1081.CrossRefPubMedGoogle Scholar
  44. Sahyoun, C., Floyer-Lea, A., Johansen-Berg, H., & Matthews, P. M. (2004). Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements. NeuroImage, 21(2), 568–575. doi: 10.1016/j.neuroimage.2003.09.065.CrossRefPubMedGoogle Scholar
  45. Salimi-Khorshidi, G., Smith, S. M., Keltner, J. R., Wager, T. D., & Nichols, T. E. (2009). Meta-analysis of neuroimaging data: a comparison of image-based and coordinate-based pooling of studies. NeuroImage, 45(3), 810–823. doi: 10.1016/j.neuroimage.2008.12.039.CrossRefPubMedGoogle Scholar
  46. Scott, S. H. (2012). The computational and neural basis of voluntary motor control and planning. Trends in Cognitive Sciences, 16(11), 541–549. doi: 10.1016/j.tics.2012.09.008.CrossRefPubMedGoogle Scholar
  47. Semrau, J. A., Herter, T. M., Scott, S. H., & Dukelow, S. P. (2013). Robotic identification of kinesthetic deficits after stroke. Stroke, 44(12), 3414–3421. doi: 10.1161/STROKEAHA.113.002058.CrossRefPubMedGoogle Scholar
  48. Semrau, J. A., Herter, T. M., Scott, S. H., & Dukelow, S. P. (2015). Examining differences in patterns of sensory and motor recovery after stroke with robotics. Stroke, 46(12), 3459–3469. doi: 10.1161/STROKEAHA.115.010750.CrossRefPubMedGoogle Scholar
  49. Sherrington, C. (1907). On the proprioceptive system, especially in its reflex aspect. Brain, 29(4), 467–485.CrossRefGoogle Scholar
  50. Stoeckel, M. C., Weder, B., Binkofski, F., Buccino, G., Shah, N. J., & Seitz, R. J. (2003). A fronto-parietal circuit for tactile object discrimination: an event-related fMRI study. NeuroImage, 19(3), 1103–1114. doi: 10.1016/S1053-8119(03)00182-4.CrossRefPubMedGoogle Scholar
  51. Stoeckel, M. C., Weder, B., Binkofski, F., Choi, H. J., Amunts, K., Pieperhoff, P., et al. (2004). Left and right superior parietal lobule in tactile object discrimination. European Journal of Neuroscience, 19(4), 1067–1072. doi: 10.1111/j.0953-816X.2004.03185.x.CrossRefPubMedGoogle Scholar
  52. Stoesz, M. R., Zhang, M., Weisser, V. D., Prather, S. C., Mao, H., & Sathian, K. (2003). Neural networks active during tactile form perception: common and differential activity during macrospatial and microspatial tasks. International Journal of Psychophysiology, 50(1–2), 41–49. doi: 10.1016/S0167-8760(03)00.CrossRefPubMedGoogle Scholar
  53. Tong, D.-M. D.-M., Zhou, Y.-T. Y.-T., Wang, G.-S. G.-S., Cheng, X.-D., Yang, T.-H. T.-H., Chang, C.-H. C.-H., & Wang, Y.-W. Y.-W. (2010). Hemorrhagic pure sensory strokes in the thalamus and Striatocapsular area: causes, clinical features and long-term outcome. European Neurology, 64(5), 275–279. doi: 10.1159/000320938.CrossRefPubMedGoogle Scholar
  54. Tsakiris, M., Longo, M. R., & Haggard, P. (2010). Having a body versus moving your body: neural signatures of agency and body-ownership. Neuropsychologia, 48(9), 2740–2749. doi: 10.1016/j.neuropsychologia.2010.05.021.CrossRefPubMedGoogle Scholar
  55. Turkeltaub, P. E., Eickhoff, S. B., Laird, A. R., Fox, M., Wiener, M., & Fox, P. (2012). Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Human Brain Mapping, 33(1), 1–13. doi: 10.1002/hbm.21186.CrossRefPubMedGoogle Scholar
  56. Tyson, S. F., Hanley, M., Chillala, J., Selley, A. B., & Tallis, R. C. (2008). Sensory loss in hospital-admitted people with stroke: characteristics, associated factors, and relationship with function. Neurorehabilitation and Neural Repair, 22(2), 166–172. doi: 10.1177/1545968307305523.CrossRefPubMedGoogle Scholar
  57. Van de Winckel, A., Sunaert, S., Wenderoth, N., Peeters, R., Van Hecke, P., Feys, H., et al. (2005). Passive somatosensory discrimination tasks in healthy volunteers: differential networks involved in familiar versus unfamiliar shape and length discrimination. NeuroImage, 26(2), 441–453. doi: 10.1016/j.neuroimage.2005.01.058.CrossRefPubMedGoogle Scholar
  58. Van de Winckel, A., Wenderoth, N., De Weerdt, W., Sunaert, S., Peeters, R., Van Hecke, W., et al. (2012). Frontoparietal involvement in passively guided shape and length discrimination: a comparison between subcortical stroke patients and healthy controls. Experimental Brain Research, 220(2), 179–189. doi: 10.1007/s00221-012-3128-2.CrossRefPubMedGoogle Scholar
  59. Weiller, C., Jüptner, M., Fellows, S., Rijntjes, M., Leonhardt, G., Kiebel, S., et al. (1996). Brain representation of active and passive movements. NeuroImage, 4(2), 105–110. doi: 10.1006/nimg.1996.0034.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Jeffrey M. Kenzie
    • 1
    • 2
    • 3
  • Ettie Ben-Shabat
    • 3
  • Gemma Lamp
    • 3
    • 4
  • Sean P. Dukelow
    • 1
    • 2
  • Leeanne M. Carey
    • 3
    • 4
  1. 1.Department of Neuroscience, Cumming School of MedicineUniversity of CalgaryCalgaryCanada
  2. 2.Hotchkiss Brain Institute, Cumming School of MedicineUniversity of CalgaryCalgaryCanada
  3. 3.Neurorehabilitation and Recovery, StrokeFlorey Institute of Neuroscience and Mental HealthMelbourneAustralia
  4. 4.Occupational Therapy, School of Allied Health, College of Science, Health and EngineeringLa Trobe UniversityMelbourneAustralia

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