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Altered cortical activation during action observation in amyotrophic lateral sclerosis patients: a parametric functional MRI study

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Abstract

Objectives

To investigate functional cerebral abnormalities in patients with amyotrophic lateral sclerosis (ALS) using functional magnetic resonance imaging (fMRI) during action observation.

Methods

Thirty patients with ALS and 30 matched healthy controls underwent fMRI with an experimental paradigm while observing a video of repetitive flexion-extension of the fingers at three frequency levels or three complexity levels, alternated with periods of a static hand. A parametric analysis was applied to determine the effects of each of the two factors.

Results

Action observation activated similar neural networks as the research on execution of action in the ALS patients and healthy subjects in several brain regions related to the mirror-neuron system (MNS). In the ALS patients, in particular, the dorsal lateral premotor cortex (dPMC), inferior parietal gyrus (IPG), and SMA, were more activated compared with the activation in the controls. Increased activation within the primary motor cortex (M1), dPMC, inferior frontal gyrus (IFG), and superior parietal gyrus (SPG) mainly correlated with hand movement frequency/complexity in the videos in the patients compared with controls.

Conclusions

The findings indicated an ongoing compensatory process occurring within the higher order motor-processing system of ALS patients, likely to overcome the loss of function.

Key Points

• Action observation activated similar core nodes of MNS in ALS and controls.

• Increased activation within M1, dPMC, IFG and SPG mainly correlated with hand movement frequency/complexity.

• Differences in patients and controls may be due to compensatory processes in ALS.

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Abbreviations

AAL:

Automated anatomical labeling

ALS:

Amyotrophic lateral sclerosis

ALSFRS-R:

Revised ALS functional rating scale

BCI:

Brain–computer interface

dPMC:

Dorsal lateral premotor cortex

EPI:

Echo-planar imaging

FLAIR:

Fluid-attenuated inversion recovery

fMRI:

Functional magnetic resonance imaging

IFG:

Inferior frontal gyrus

M1:

primary motor cortex

MNS:

Mirror neuron system

MPRAGE:

Magnetization prepared rapid acquisition of gradient echo

SMA:

Supplementary motor area

SPM8:

Statistical Parametric Mapping 8

SPG:

Superior parietal gyrus

References

  1. Wijesekera LC, Leigh PN (2009) Amyotrophic lateral sclerosis. Orphanet J Rare Dis 4:3

    Article  PubMed Central  PubMed  Google Scholar 

  2. Konrad C, Henningsen H, Bremer J et al (2002) Pattern of cortical reorganization in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study. Exp Brain Res 143:51–56

    Article  PubMed  Google Scholar 

  3. Konrad C, Jansen A, Henningsen H et al (2006) Subcortical reorganization in amyotrophic lateral sclerosis. Exp Brain Res 172:361–369

    Article  CAS  PubMed  Google Scholar 

  4. Schoenfeld MA, Tempelmann C, Gaul C et al (2005) Functional motor compensation in amyotrophic lateral sclerosis. J Neurol 252:944–952

    Article  PubMed  Google Scholar 

  5. Tessitore A, Esposito F, Monsurro MR et al (2006) Subcortical motor plasticity in patients with sporadic ALS: An fMRI study. Brain Res Bull 69:489–494

    Article  CAS  PubMed  Google Scholar 

  6. Stanton BR, Williams VC, Leigh PN et al (2007) Altered cortical activation during a motor task in ALS. Evidence for involvement of central pathways. J Neurol 254:1260–1267

    Article  PubMed  Google Scholar 

  7. Decety J, Grezes J (1999) Neural mechanisms subserving the perception of human actions. Trends Cogn Sci 3:172–178

    Article  PubMed  Google Scholar 

  8. Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 14:S103–S109

    Article  CAS  PubMed  Google Scholar 

  9. Caspers S, Zilles K, Laird AR, Eickhoff SB (2010) ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50:1148–1167

    Article  PubMed  Google Scholar 

  10. Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res 3:131–141

    Article  CAS  PubMed  Google Scholar 

  11. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119(Pt 2):593–609

    Article  PubMed  Google Scholar 

  12. Buccino G, Binkofski F, Riggio L (2004) The mirror neuron system and action recognition. Brain Lang 89:370–376

    Article  PubMed  Google Scholar 

  13. Cattaneo L, Rizzolatti G (2009) The mirror neuron system. Arch Neurol 66:557–560

    Article  PubMed  Google Scholar 

  14. Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron D (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293–299

    Article  CAS  PubMed  Google Scholar 

  15. Cedarbaum JM, Stambler N, Malta E et al (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 169:13–21

    Article  CAS  PubMed  Google Scholar 

  16. Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC (1996) A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4:58–73

    Article  CAS  PubMed  Google Scholar 

  17. Tzourio-Mazoyer N, Landeau B, Papathanassiou D et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289

    Article  CAS  PubMed  Google Scholar 

  18. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192

    Article  CAS  PubMed  Google Scholar 

  19. Gazzola V, Keysers C (2009) The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cereb Cortex 19:1239–1255

    Article  PubMed Central  PubMed  Google Scholar 

  20. Blakemore SJ, Bristow D, Bird G, Frith C, Ward J (2005) Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. Brain 128:1571–1583

    Article  PubMed  Google Scholar 

  21. Keysers C, Wicker B, Gazzola V, Anton JL, Fogassi L, Gallese V (2004) A touching sight: SII/PV activation during the observation and experience of touch. Neuron 42:335–346

    Article  CAS  PubMed  Google Scholar 

  22. Chouinard PA, Paus T (2006) The primary motor and premotor areas of the human cerebral cortex. Neuroscientist 12:143–152

    Article  PubMed  Google Scholar 

  23. Hoshi E, Tanji J (2004) Functional specialization in dorsal and ventral premotor areas. Prog Brain Res 143:507–511

    Article  PubMed  Google Scholar 

  24. Hoshi E, Tanji J (2007) Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties. Curr Opin Neurobiol 17:234–242

    Article  CAS  PubMed  Google Scholar 

  25. Rozzi S, Ferrari PF, Bonini L, Rizzolatti G, Fogassi L (2008) Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. Eur J Neurosci 28:1569–1588

    Article  PubMed  Google Scholar 

  26. Bremmer F, Schlack A, Shah NJ et al (2001) Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron 29:287–296

    Article  CAS  PubMed  Google Scholar 

  27. Ohara S, Ikeda A, Kunieda T et al (2000) Movement-related change of electrocorticographic activity in human supplementary motor area proper. Brain 123(Pt 6):1203–1215

    Article  PubMed  Google Scholar 

  28. Dum RP, Strick PL (1996) Spinal cord terminations of the medial wall motor areas in macaque monkeys. J Neurosci 16:6513–6525

    CAS  PubMed  Google Scholar 

  29. Lule D, Diekmann V, Kassubek J et al (2007) Cortical plasticity in amyotrophic lateral sclerosis: motor imagery and function. Neurorehabil Neural Repair 21:518–526

    Article  PubMed  Google Scholar 

  30. Stanton BR, Williams VC, Leigh PN et al (2007) Cortical activation during motor imagery is reduced in Amyotrophic Lateral Sclerosis. Brain Res 1172:145–151

    Article  CAS  PubMed  Google Scholar 

  31. Moran DW, Schwartz AB (1999) Motor cortical representation of speed and direction during reaching. J Neurophysiol 82:2676–2692

    CAS  PubMed  Google Scholar 

  32. Johnson MT, Coltz JD, Ebner TJ (1999) Encoding of target direction and speed during visual instruction and arm tracking in dorsal premotor and primary motor cortical neurons. Eur J Neurosci 11:4433–4445

    Article  CAS  PubMed  Google Scholar 

  33. Kawashima R, Inoue K, Sugiura M, Okada K, Ogawa A, Fukuda H (1999) A positron emission tomography study of self-paced finger movements at different frequencies. Neuroscience 92:107–112

    Article  CAS  PubMed  Google Scholar 

  34. Jancke L, Specht K, Mirzazade S et al (1998) A parametric analysis of the ‘rate effect’ in the sensorimotor cortex: a functional magnetic resonance imaging analysis in human subjects. Neurosci Lett 252:37–40

    Article  CAS  PubMed  Google Scholar 

  35. Hayashi MJ, Saito DN, Aramaki Y, Asai T, Fujibayashi Y, Sadato N (2008) Hemispheric asymmetry of frequency-dependent suppression in the ipsilateral primary motor cortex during finger movement: a functional magnetic resonance imaging study. Cereb Cortex 18:2932–2940

    Article  PubMed Central  PubMed  Google Scholar 

  36. Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund H (1999) A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur J Neurosci 11:3276–3286

    Article  CAS  PubMed  Google Scholar 

  37. 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 18:2775–2788

    Article  PubMed Central  PubMed  Google Scholar 

  38. Higashi S, Hioki K, Kurotani T, Kasim N, Molnar Z (2005) Functional thalamocortical synapse reorganization from subplate to layer IV during postnatal development in the reeler-like mutant rat (shaking rat Kawasaki). J Neurosci 25:1395–1406

    Article  CAS  PubMed  Google Scholar 

  39. Koechlin E, Jubault T (2006) Broca's area and the hierarchical organization of human behavior. Neuron 50:963–974

    Article  CAS  PubMed  Google Scholar 

  40. Harrington DL, Rao SM, Haaland KY et al (2000) Specialized neural systems underlying representations of sequential movements. J Cogn Neurosci 12:56–77

    Article  CAS  PubMed  Google Scholar 

  41. Pammi VS, Miyapuram KP, Samejima K, Ahmed, Bapi RS, Doya K (2012) Changing the structure of complex visuo-motor sequences selectively activates the fronto-parietal network. Neuroimage 59:1180–1189

    Article  PubMed  Google Scholar 

  42. Haslinger B, Erhard P, Weilke F et al (2002) The role of lateral premotor-cerebellar-parietal circuits in motor sequence control: a parametric fMRI study. Brain Res Cogn Brain Res 13:159–168

    Article  PubMed  Google Scholar 

  43. Hoover JE, Strick PL (1999) The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneuronal transport of herpes simplex virus type 1. J Neurosci 19:1446–1463

    CAS  PubMed  Google Scholar 

  44. Serrien DJ, Nirkko AC, Lovblad KO, Wiesendanger M (2001) Damage to the parietal lobe impairs bimanual coordination. Neuroreport 12:2721–2724

    Article  CAS  PubMed  Google Scholar 

  45. Ehrsson HH, Spence C, Passingham RE (2004) That's my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science 305:875–877

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The scientific guarantor of this publication is Daoying Geng. The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. Approval from the institutional animal care committee was not required because our study is on human subjects. No study subjects or cohorts have been previously reported. Methodology: case–control study.

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Authors and Affiliations

  1. Department of Radiology, Fudan University, Huashan Hospital, Shanghai, China

    Haiqing Li, Yuxin Li, Bo Yin, Weijun Tang, Xiangrong Yu & Daoying Geng

  2. Department of Neurology, Huashan Hospital, Fudan University, Shanghai, China

    Yan Chen

  3. Department of Radiology, People’s Hospital of Hainan Province, Haikou, Hainan Province, China

    Weiyuan Huang

  4. Department of radiotherapy, Affiliated Jiangsu Province Hospital of Traditional Chinese Medicine, Nanjing University of Traditional Chinese Medicine, Nanjing, China

    Biyun Zhang

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  1. Haiqing Li
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Correspondence to Daoying Geng or Biyun Zhang.

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Li, H., Chen, Y., Li, Y. et al. Altered cortical activation during action observation in amyotrophic lateral sclerosis patients: a parametric functional MRI study. Eur Radiol 25, 2584–2592 (2015). https://doi.org/10.1007/s00330-015-3671-x

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  • DOI: https://doi.org/10.1007/s00330-015-3671-x

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