No effect of triple-pulse TMS medial to intraparietal sulcus on online correction for target perturbations during goal-directed hand and foot reaches


Autoři: Daniel S. Marigold aff001;  Kim Lajoie aff001;  Tobias Heed aff002
Působiště autorů: Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, British Columbia, Canada aff001;  Biopsychology and Cognitive Neuroscience, Faculty of Psychology and Sports Science, Bielefeld University, Bielefeld, Germany aff002;  Center of Excellence Cognitive Interaction Technology, Bielefeld University, Bielefeld, Germany aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223986

Souhrn

Posterior parietal cortex (PPC) is central to sensorimotor processing for goal-directed hand and foot movements. Yet, the specific role of PPC subregions in these functions is not clear. Previous human neuroimaging and transcranial magnetic stimulation (TMS) work has suggested that PPC lateral to the intraparietal sulcus (IPS) is involved in directing the arm, shaping the hand, and correcting both finger-shaping and hand trajectory during movement. The lateral localization of these functions agrees with the comparably lateral position of the hand and fingers within the motor and somatosensory homunculi along the central sulcus; this might suggest that, in analogy, (goal-directed) foot movements would be mediated by medial portions of PPC. However, foot movement planning activates similar regions for both hand and foot movement along the caudal-to-rostral axis of PPC, with some effector-specificity evident only rostrally, near the central regions of sensorimotor cortex. Here, we attempted to test the causal involvement of PPC regions medial to IPS in hand and foot reaching as well as online correction evoked by target displacement. Participants made hand and foot reaches towards identical visual targets. Sometimes, the target changed position 100–117 ms into the movement. We disturbed cortical processing over four positions medial to IPS with three pulses of TMS separated by 40 ms, both during trials with and without target displacement. We timed TMS to disrupt reach execution and online correction. TMS did not affect endpoint error, endpoint variability, or reach trajectories for hand or foot. While these negative results await replication with different TMS timing and parameters, we conclude that regions medial to IPS are involved in planning, rather than execution and online control, of goal-directed limb movements.

Klíčová slova:

Body limbs – Ellipses – Feet – Fingers – Functional magnetic resonance imaging – Hands – Toes – Transcranial magnetic stimulation


Zdroje

1. Andersen RA, Cui H. Intention, action planning, and decision making in parietal-frontal circuits. Neuron. 2009;63: 568–583. doi: 10.1016/j.neuron.2009.08.028 19755101

2. Vesia M, Crawford JD. Specialization of reach function in human posterior parietal cortex. Exp Brain Res. 2012;221: 1–18. doi: 10.1007/s00221-012-3158-9 22777102

3. Filimon F. Human cortical control of hand movements: parietofrontal networks for reaching, grasping, and pointing. Neuroscientist. 2010;16: 388–407. doi: 10.1177/1073858410375468 20817917

4. Heed T, Beurze SM, Toni I, Röder B, Medendorp WP. Functional rather than effector-specific organization of human posterior parietal cortex. J Neurosci. 2011;31: 3066–3076. doi: 10.1523/JNEUROSCI.4370-10.2011 21414927

5. Leoné FTM, Heed T, Toni I, Medendorp WP. Understanding effector selectivity in human posterior parietal cortex by combining information patterns and activation measures. J Neurosci. 2014;34: 7102–7112. doi: 10.1523/JNEUROSCI.5242-13.2014 24849346

6. Cunningham DA, Machado A, Yue GH, Carey JR, Plow EB. Functional somatotopy revealed across multiple cortical regions using a model of complex motor task. Brain Res. 2013;1531: 25–36. doi: 10.1016/j.brainres.2013.07.050 23920009

7. Heed T, Leone FTM, Toni I, Medendorp WP. Functional versus effector-specific organization of the human posterior parietal cortex: revisited. J Neurophysiol. 2016;116: 1885–1899. doi: 10.1152/jn.00312.2014 27466132

8. Rijntjes M, Dettmers C, Büchel C, Kiebel S, Frackowiak RSJ, Weiller C. A blueprint for movement: functional and anatomical representations in the human motor system. J Neurosci. 1999;19: 8043–8048. 10479704

9. Miall RC, Wolpert DM. Forward models for physiological motor control. Neural Net. 1996;9: 1265–1279.

10. Mulliken GH, Musallam S, Andersen RA. Forward estimation of movement state in posterior parietal cortex. Proc Natl Acad Sci USA. 2008;105: 8170–8177. doi: 10.1073/pnas.0802602105 18499800

11. Wolpert DM, Goodbody SJ, Husain M. Maintaining internal representations: the role of the human superior parietal lobe. Nat Neurosci. 1998;1: 529–533. doi: 10.1038/2245 10196553

12. Buneo CA, Andersen RA. The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia. 2006; 44: 2594–2606. doi: 10.1016/j.neuropsychologia.2005.10.011 16300804

13. Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE, Grafton ST. Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat Neurosci. 1999;2: 563–567. doi: 10.1038/9219 10448222

14. Drew T, Marigold DS. Taking the next step: cortical contributions to the control of locomotion. Curr Opin Neurobiol. 2015;33: 25–33. doi: 10.1016/j.conb.2015.01.011 25643847

15. Marigold DS, Drew T. Posterior parietal cortex estimates the relationship between object and body location during locomotion. eLife. 2017;6:e28143. doi: 10.7554/eLife.28143 29053442

16. Marigold DS, Andujar J-E, Lajoie K, Drew T. Motor planning of locomotor adaptations on the basis of vision: the role of the posterior parietal cortex. Prog Brain Res. 2011;188: 83–100. doi: 10.1016/B978-0-444-53825-3.00011-5 21333804

17. Danckert J, Ferber S, Goodale MA. Direct effects of prismatic lenses on visuomotor control: an event-related functional MRI study. Eur J Neurosci. 2008;28: 1696–1704. doi: 10.1111/j.1460-9568.2008.06460.x 18973586

18. Luauté J, Schwartz S, Rossetti Y, Spiridon M, Rode G, Boisson D, et al. Dynamic changes in brain activity during prism adaptation. J Neurosci. 2009;29: 169–178. doi: 10.1523/JNEUROSCI.3054-08.2009 19129395

19. Archambault PS, Caminiti R, Battaglia-Mayer A. Cortical mechanisms for online control of hand movement trajectory: the role of the posterior parietal cortex. Cereb Cortex. 2009;19: 2848–2864. doi: 10.1093/cercor/bhp058 19359349

20. Archambault PS, Ferrari-Toniolo S, Battaglia-Mayer A. Online control of hand trajectory and evolution of motor intention in the parietofrontal system. J Neurosci. 2011;31: 742–752. doi: 10.1523/JNEUROSCI.2623-10.2011 21228183

21. Marigold DS, Drew T. Contribution of cells in the posterior parietal cortex to the planning of visually guided locomotion in the cat: effects of temporary visual interruption. J Neurophysiol. 2011;105: 2457–2470. doi: 10.1152/jn.00992.2010 21411565

22. Gréa H, Pisella L, Rossetti Y, Desmurget M, Tilikete C, Grafton S, et al. A lesion of the posterior parietal cortex disrupts on-line adjustments during aiming movements. Neuropsychologia. 2002;40: 2471–2480. doi: 10.1016/s0028-3932(02)00009-x 12417474

23. Tunik E, Frey SH, Grafton ST. Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp. Nat Neurosci. 2005;8: 505–511. doi: 10.1038/nn1430 15778711

24. Reichenbach A, Bresciani J-P, Peer A, Bülthoff HH, Thielscher A. Contributions of the PPC to online control of visually guided reaching movements assessed with fMRI-guided TMS. Cereb Cortex. 2011;21: 1602–1612. doi: 10.1093/cercor/bhq225 21084453

25. Sandrini M, Umiltà C, Rusconi E. The use of transcranial magnetic stimulation in cognitive neuroscience: A new synthesis of methodological issues. Neurosci Biobehav Rev. 2011;35: 516–536. doi: 10.1016/j.neubiorev.2010.06.005 20599555

26. Hagler DJ Jr, Riecke L, Sereno MI. Parietal and superior frontal visuospatial maps activated by pointing and saccades. NeuroImage. 2007;35: 1562–1577. doi: 10.1016/j.neuroimage.2007.01.033 17376706

27. Levy I, Schluppeck D, Heeger DJ, Glimcher PW. Specificity of human cortical areas for reaches and saccades. J Neurosci. 2007;27: 4687–4696. doi: 10.1523/JNEUROSCI.0459-07.2007 17460081

28. Schluppeck D, Glimcher P, Heeger DJ. Topographic organization for delayed saccades in human posterior parietal cortex. J Neurophysiol. 2005;94: 1372–1384. doi: 10.1152/jn.01290.2004 15817644

29. Silver MA, Ress D, Heeger DJ. Topographic maps of visual spatial attention in human parietal cortex. J Neurophysiol. 2005;94: 1358–1371. doi: 10.1152/jn.01316.2004 15817643

30. Filimon F, Nelson JD, Huang R-S, Sereno MI. Multiple parietal reach regions in humans: cortical representations for visual and proprioceptive feedback during on-line reaching. J Neurosci. 2009;29: 2961–2971. doi: 10.1523/JNEUROSCI.3211-08.2009 19261891

31. Prado J, Clavagnier S, Otzenberger H, Scheiber C, Kennedy H, Perenin MT. Two cortical systems for reaching in central and peripheral vision. Neuron. 2005;48: 849–858. doi: 10.1016/j.neuron.2005.10.010 16337921

32. Vesia M, Prime SL, Yan X, Sergio LE, Crawford JD. Specificity of human parietal saccade and reach regions during transcranial magnetic stimulation. J Neurosci. 2010;30: 13053–13065. doi: 10.1523/JNEUROSCI.1644-10.2010 20881123

33. Blangero A, Menz MM, McNamara A, Binkofski F. Parietal modules for reaching. Neuropsychologia. 2009;47: 1500–1507. doi: 10.1016/j.neuropsychologia.2008.11.030 19109986

34. Glover S, Miall RC, Rushworth MFS. Parietal rTMS disrupts the initiation but not the execution of on-line adjustments to a perturbation of object size. J Cogn Neurosci. 2005;17: 124–136. doi: 10.1162/0898929052880066 15701244

35. Le A, Vesia M, Yan X, Crawford JD, Niemeier M. Parietal area BA7 integrates motor programs for reaching, grasping, and bimanual coordination. J Neurophysiol. 2017;117: 624–636. doi: 10.1152/jn.00299.2016 27832593

36. Striemer CL, Chouinard PA, Goodale MA. Programs for action in superior parietal cortex: a triple-pulse TMS investigation. Neuropsychologia. 2011;49: 2391–2399. doi: 10.1016/j.neuropsychologia.2011.04.015 21539851

37. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, the Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009;120: 2008–2039. doi: 10.1016/j.clinph.2009.08.016 19833552

38. Schubert P, Kirchner M. Ellipse area calculations and their applicability in posturography. Gait Posture. 2014;39: 518–522. doi: 10.1016/j.gaitpost.2013.09.001 24091249

39. Davare M, Zénon A, Desmurget M, Olivier E. Dissociable contribution of the parietal and frontal cortex to coding movement direction and amplitude. Front Hum Neurosci. 2015;9.

40. Reichenbach A, Bresciani J-P, Bülthoff HH, Thielscher A. Reaching with the sixth sense: vestibular contributions to voluntary motor control in the human right parietal cortex. NeuroImage. 2016;124: 869–875. doi: 10.1016/j.neuroimage.2015.09.043 26424179

41. Scott SH. A Functional taxonomy of bottom-up sensory feedback processing for motor actions. Trends Neurosci. 2016;39: 512–526. doi: 10.1016/j.tins.2016.06.001 27378546

42. Serra C, Galletti C, Marco SD, Fattori P, Galati G, Sulpizio V, et al. Egomotion-related visual areas respond to active leg movements. Hum Brain Mapp. doi: 10.1002/hbm.24589 30924264

43. Beurze SM, de Lange FP, Toni I, Medendorp WP. Spatial and effector processing in the human parietofrontal network for reaches and saccades. J Neurophysiol. 2009;101: 3053–3062. doi: 10.1152/jn.91194.2008 19321636

44. Tosoni A, Galati G, Romani GL, Corbetta M. Sensory-motor mechanisms in human parietal cortex underlie arbitrary visual decisions. Nat Neurosci. 2008;11: 1446–1453. doi: 10.1038/nn.2221 18997791

45. Fernandez-Ruiz J, Goltz HC, DeSouza JFX, Vilis T, Crawford JD. Human parietal “reach region” primarily encodes intrinsic visual direction, not extrinsic movement direction, in a visual-motor dissociation task. Cereb Cortex. 2007;17: 2283–2292. doi: 10.1093/cercor/bhl137 17215478

46. Medendorp WP, Goltz HC, Crawford JD, Vilis T. Integration of target and effector information in human posterior parietal cortex for the planning of action. J Neurophysiol. 2005;93: 954–962. doi: 10.1152/jn.00725.2004 15356184

47. Pellijeff A, Bonilha L, Morgan PS, McKenzie K, Jackson SR. Parietal updating of limb posture: an event-related fMRI study. Neuropsychologia. 2006;44: 2685–2690. doi: 10.1016/j.neuropsychologia.2006.01.009 16504223

48. Leib R, Mawase F, Karniel A, Donchin O, Rothwell J, Nisky I, et al. Stimulation of PPC affects the mapping between motion and force signals for stiffness perception but not motion control. J Neurosci. 2016;36: 10545–10559. doi: 10.1523/JNEUROSCI.1178-16.2016 27733607

49. Taoka M, Toda T, Iwamura Y. Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex. Exp Brain Res. 1998;123: 315–322. doi: 10.1007/s002210050574 9860270

50. Breveglieri R, Galletti C, Gamberini M, Passarelli L, Fattori P. Somatosensory cells in area PEc of macaque posterior parietal cortex. J Neurosci. 2006;26: 3679–3684. doi: 10.1523/JNEUROSCI.4637-05.2006 16597722

51. Breveglieri R, Galletti C, Monaco S, Fattori P. Visual, somatosensory, and bimodal activities in the macaque parietal area PEc. Cereb Cortex. 2008;18, 806–816. doi: 10.1093/cercor/bhm127 17660487

52. Tunik E, Rice NJ, Hamilton A, Grafton ST. Beyond grasping: representation of action in human anterior intraparietal sulcus. NeuroImage. 2007;36: T77–T86. doi: 10.1016/j.neuroimage.2007.03.026 17499173

53. Zhang CY, Aflalo T, Revechkis B, Rosario ER, Ouellette D, Pouratian N, et al. Partially mixed selectivity in human posterior parietal association cortex. Neuron. 2017;95, 697–708. doi: 10.1016/j.neuron.2017.06.040 28735750


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