Probing the reaching–grasping network in humans through multivoxel pattern decoding

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Introduction:
The quest for a putative human homolog of the reaching–grasping network identified in monkeys has been the focus of many neuropsychological and neuroimaging studies in recent years. These studies have shown that the network underlying reaching-only and reach-to-grasp movements includes the superior parieto-occipital cortex (SPOC), the anterior part of the human intraparietal sulcus (hAIP), the ventral and the dorsal portion of the premotor cortex, and the primary motor cortex (M1). Recent evidence for a wider frontoparietal network coding for different aspects of reaching-only and reach-to-grasp actions calls for a more fine-grained assessment of the reaching–grasping network in humans by exploiting pattern decoding methods (multivoxel pattern analysis—MVPA).

Methods:
Here, we used MPVA on functional magnetic resonance imaging (fMRI) data to assess whether regions of the frontoparietal network discriminate between reaching-only and reach-to-grasp actions, natural and constrained grasping, different grasp types, and object sizes. Participants were required to perform either reaching-only movements or two reach-to-grasp types (precision or whole hand grasp) upon spherical objects of different sizes.

Results:
Multivoxel pattern analysis highlighted that, independently from the object size, all the selected regions of both hemispheres contribute in coding for grasp type, with the exception of SPOC and the right hAIP. Consistent with recent neurophysiological findings on monkeys, there was no evidence for a clear-cut distinction between a dorsomedial and a dorsolateral pathway that would be specialized for reaching-only and reach-to-grasp actions, respectively. Nevertheless, the comparison of decoding accuracy across brain areas highlighted their different contributions to reaching-only and grasping actions.

Conclusions:
Altogether, our findings enrich the current knowledge regarding the functional role of key brain areas involved in the cortical control of reaching-only and reach-to-grasp actions in humans, by revealing novel fine-grained distinctions among action types within a wide frontoparietal network.

Keywords:
Functional magnetic resonance imaging; multivoxel pattern decoding; reaching-only action; visuomotor reach-to-grasp action

Autoři: Maria Grazia Di Bono ^1,*; Chiara Begliomini ^1,2; Umberto Castiello Andmarco Zorzi ^{1,2,3 1,2,4,*}
Vyšlo v časopise: Brain and Behavior, 11, 2015, č. 5, s. 1-18
prolekare.web.journal.doi_sk: https://doi.org/10.1002/brb3.412

© 2015 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Souhrn

Keywords:
Functional magnetic resonance imaging; multivoxel pattern decoding; reaching-only action; visuomotor reach-to-grasp action

Zdroje

1. Amunts, K., and K. Zilles. 2001. Advances in cytoarchitectonic mapping of the human cerebral cortex. Neuroimaging Clin. N. Am. 11:151–169. PubMed,Web of Science® Times Cited: 85

2. Amunts, K., A. Schleicher, U. Bürgel, H. Mohlberg, H. B. Uylings, and K. Zilles. 1999. Broca's region revisited: cytoarchitecture and intersubject variability. J. Comp. Neurol. 412:319–341.

3. Begliomini, C., M. B. Wall, A. T. Smith, and U. Castiello. 2007a. Differential cortical activity for precision and whole-hand visually guided grasping in humans. Eur. J. Neurosci. 25:1245–1252.

4. Begliomini, C., A. Caria, W. Grodd, and U. Castiello. 2007b. Comparing natural and constrained movements: new insight into the visuomotor control of grasping. PLoS One 2:e1108.

5. Begliomini, C., C. Nelini, A. Caria, W. Grodd, and U. Castiello. 2008. Cortical activations in humans grasp-related areas depend on hand used and handedness. PLoS One 3:e3388.

6. Begliomini, C., T. De Sanctis, M. Marangon, V. Tarantino, L. Sartori, D. Miotto, et al. 2014. An investigation of the neural circuits underlying reaching and reach-to-grasp movements: from planning to execution. Front. Hum. Neurosci. 8:676.

7. Binkofski, F., G. Buccino, S. Posse, R. J. Seitz, G. Rizzolatti, and A. Freund. 1999. Fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur. J. Neurosci. 11:3276–3286.

8. Boroojerdi, B., K. Diefenbach, and A. Ferbert. 1996. Transcallosal inhibition in cortical and subcortical cerebral vascular lesions. J. Neurol. Sci. 144:160–170.

9. Bremmer, F., A., Schlack, N. J., Shah, O., Zafiris, M., Kubischik, K. P., Hoffmann, K., Zilles, and G. R. Fink. 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.

10. Carpaneto, J., M. A. Umiltà, L. Fogassi, A. Murata, V. Gallese, S. Micera, et al. 2011. Decoding the activity of grasping neurons recorded from the ventral premotor area F5 of the macaque monkey. Neuroscience 188:80–94.

11. Castiello, U. 2005. The neuroscience of grasping. Nat. Rev. Neurosci. 6:726–736.

12. Castiello, U., and C. Begliomini. 2008. The cortical control of visually guided grasping. Neuroscientist 14:157–170.

13. Cavina-Pratesi, C., M. Goodale, and J. C. Culham. 2007. FMRI reveals a dissociation between grasping and perceiving the size of real 3D objects. PLoS One 5:1–14.

14. Cavina-Pratesi, C., S. Monaco, P. Fattori, C. Galletti, T. D. McAdam, D. J. Quinlan, et al. 2010. Functional magnetic resonance imaging reveals the neural substrates of arm transport and grip formation in reach-to-grasp actions in humans. J. Neurosci.30:10306–10323.

15. Chen, Y., P. Namburi, L. T. Elliott, J. Heinzle, C. S. Soon, M. W. Chee, et al. 2011. Cortical surface-based searchlight decoding.NeuroImage 56:582–592.

16. Choi, H. J., K. Zilles, H. Mohlberg, A. Schleicher, G. R. Fink, E. Armstrong, et al. 2006. Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus. J. Comp. Neurol. 495:53–69.

17. Culham, J. C., S. L. Danckert, J. F. DeSouza, J. S. Gati, R. S. Menon, and M. A. Goodale. 2003. Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp. Brain Res. 153:180–189.

18. Culham, J. C., C. Cavina-Pratesi, and A. Singhal. 2006. The role of parietal cortex in visuomotor control: what have we learned from neuroimaging? Neuropsychologia 44:2668–2684.

19. Davare, M., M. Andrei, G. Cosnard, J. L. Thonnard, and E. Olivier. 2006. Dissociating the role of ventral and dorsal premotor cortex in precision grasping. J. Neurosci. 26:2260–2268.

20. Davare, M., J. Duque, Y. Vandermeeren, J. L. Thonnard, and E. Olivier. 2007. Role of the ipsilateral primary motor cortex in controlling the timing of hand muscle recruitment. Cereb. Cortex 17:353–362.

21. Davare, M., R. Lemon, and E. Olivier. 2008. Selective modulation of interactions between ventral premotor cortex and primary motor cortex during precision grasping in humans. J. Physiol. 586:2735–2742.

22. Davare, M., J. C. Rothwell, and R. N. Lemon. 2010. Causal connectivity between the human anterior intraparietal area and premotor cortex during grasp. Curr. Biol. 20:176–181.

23. Di Bono, M. G., and M. Zorzi. 2008. Decoding cognitive states from fMRI data using support vector regression. PsychNol. J. 6:189201.

24. Di Lazzaro, V., A. Oliviero, P. Profice, A. Insola, P. Mazzone, P. Tonali, et al. 1999. Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation. Exp. Brain Res. 124:520–524.

25. Duhamel, J. R., C. L. Colby, and M. E. Goldberg. 1998. Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J. Neurophysiol. 79:126–136.

26. Ehrsson, H. H., A. Fagergren, T. Jonsson, G. Westling, R. S. Johansson, and H. Forssberg. 2000. Cortical activity in precision- versus power-grip tasks: an fMRI study. J. Neurophysiol. 83:528–536.

27. Ehrsson, H. H., E. Fagergren, and H. Forssberg. 2001. Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI Study. J. Neurophysiol. 85:2613–2623.

28. Fabbri, S., A. Caramazza, and A. Lingnau. 2012. Distributed sensitivity for movement amplitude in directionally tuned neuronal populations. J. Neurophysiol. 107:1845–1856.

29. Fabbri, S., L. Strnad, A. Caramazza, and A. Lingnau. 2014. Overlapping representations for grip type and reach direction. NeuroImage94:138–146.

30. Fagg, A. H., and M. A. Arbib. 1998. Modeling parietal-premotor interactions in primate control of grasping. Neural Netw.11:1277–1303.

31. Fattori, P., R. Breveglieri, N. Marzocchi, D. Filippini, A. Bosco, and C. Galletti. 2009. Hand orientation during reach-to-grasp movements modulates neuronal activity in the medial posterior parietal area V6A. J. Neurosci. 29:1928–1936.

32. Fattori, P., V. Raos, R. Breveglieri, A. Bosco, N. Marzocchi, and C. Galletti. 2010. The dorsomedial pathway is not just for reaching: grasping neurons in the medial parieto-occipital cortex of the macaque monkey. J. Neurosci. 30:342–349.

33. Fattori, P., R. Breveglieri, V. Raos, A. Bosco, and C. Galletti. 2012. Vision for action in the macaque medial posterior parietal cortex. J. Neurosci. 32:3221–3234.

34. Filimon, F. 2010. Human cortical control of hand movements: parietofrontal networks for reaching, grasping, and pointing.Neuroscientist 16:388–407.

35. Filimon, F., J. D. Nelson, R. S. Huang, and M. I. Sereno. 2009. Multiple parietal reach regions in humans: cortical representations for visual and proprioceptive feedback during on-line reaching. J. Neurosci. 29:2961–2971.

36. Frey, H. S., D. Vinton, R. Norlund, and S. T. Grafton. 2005. Cortical topography of human anterior intraparietal cortex active during visually guided grasping. Cogn. Brain Res. 23:397–405.

37. Galletti, C., D. F. Kutz, M. Gamberini, R. Breveglieri, and P. Fattori. 2003. Role of the medial parieto-occipital cortex in the control of reaching and grasping movements. Exp. Brain Res. 153:158–170.

38. Gallivan, J. P., D. A. McLean, K. F. Valyear, C. E. Pettypiece, and J. C. Culham. 2011. Decoding action intentions from preparatory brain activity in human parieto-frontal networks. J. Neurosci. 31:9599–9610.

39. Gardner, E. P., K. S. Babu, S. D. Reitzen, S. Ghosh, A. S. Brown, J. Chen, et al. 2007. Neurophysiology of prehension. I. Posterior parietal cortex and object-oriented hand behaviors. J. Neurophysiol. 97:387–406.

40. Geyer, S. 2003. Brodmanns areas. Pp. 482–496 in M. J. Aminoff and R. B. Daroff, eds. Encyclopedia of the neurological sciences. Academic Press, San Diego.

41. Geyer, S., A. Ledberg, A. Schleicher, S. Kinomura, T. Schormann, U. Bürgel, et al. 1996. Two different areas within the primary motor cortex of man. Nature 382:805–807.

42. Geyer, S., A. Schleicher, and K. Zilles. 1999. Areas 3a, 3b, and 1 of human primary somatosensory cortex: 1. Microstructural organization and interindividual variability. NeuroImage 10:63–83.

43. Geyer, S., T. Schormann, H. Mohlberg, and K. Zilles. 2000. Areas 3a, 3b, and 1 of human primary somatosensory cortex: 2. Spatial normalization to standard anatomical space. NeuroImage 11:684–696.

44. Glover, S., R. C. Miall, and M. F. S. Rushworth. 2005. Parietal rTMS disrupts the initiation but not the execution of on-line adjustments to a perturbation of object size. J. Cogn. Neurosci. 17:124–136.

45. Godschalk, M., R. N. Lemon, H. G. Nijs, and H. G. Kuypers. 1981. Behaviour of neurons in monkey peri-arcuate and precentral cortex before and during visually guided arm and hand movements. Exp. Brain Res. 44:113–116.

46. Grafton, S. T., M. A. Arbib, L. Fadiga, and G. Rizzolatti. 1996. Localization of grasp representations in humans by positron emission tomography. Exp. Brain Res. 112:103–111.

47. Grefkes, C., S. Geyer, T. Schormann, P. Roland, and K. Zilles. 2001. Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. NeuroImage 14:617–631.

48. Grol, M. J., J. Majdandzić, K. E. Stephan, L. Verhagen, H. C. Dijkerman, H. Bekkering, et al. 2007. Parieto-frontal connectivity during visually guided grasping. J. Neurosci. 27:11877–11887.

49. Hagberg, G. E., G. Zito, F. Patria, and J. N. Sanes. 2001. Improved detection of event-related functional MRI signals using probability functions. NeuroImage 14:1193–1205.

50. Hinkley, L. B., L. A. Krubitzer, J. Padberg, and E. A. Disbrow. 2009. Visual-manual exploration and posterior parietal cortex in humans.J. Neurophysiol. 102:3433–3446.

51. Jeannerod, M. 1981. Specialized channels for cognitive responses. Cognition 10:135–137.

52. Jeannerod, M., M. A., Arbib, G., Rizzolatti, and H., Sakata. 1995. Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18:314-320.

53. Jimura, K., and R. A. Poldrack. 2012. Analyses of regional-average activation and multivoxel pattern information tell complementary stories. Neuropsychologia 50:544–552.

54. Kriegeskorte, N., W. K. Simmons, P. S. F. Bellgowan, and C. I. Baker. 2009. Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 12:535–540.

55. Kroliczak, G., C. Cavina-Pratesi, D. A. Goodman, and J. C. Culham. 2007. What does the brain do when you fake it? An FMRI study of pantomimed and real grasping. J. Neurophysiol. 97:2410–2422.

56. Kuhtz-Buschbeck, J. P., R., Gilster, S., Wolff, S., Ulmer, H., Siebner, and O. Jansen. 2008. Brain activity is similar during precision and power gripping with light force: an fMRI study. Neuroimage 40:1469-1481.

57. Lawrence, D. G., and D. A. Hopkins. 1976. The development of motor control in the rhesus monkey: evidence concerning the role of corticomotoneuronal connections. Brain 99:235–254.

58. Luppino, G., A. Murata, P. Govoni, and M. Matelli. 1999. Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4). Exp. Brain Res. 128:181–187.

59. Mars, R. B., S. Jbabdi, J. Sallet, J. X. O' Reilly, P. L. Croxson, E. Olivier, et al. 2011. Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J. Neurosci. 31:4087–4100.

60. Matelli, M., and G. Luppino. 2001. Parietofrontal circuits for action and space perception in the macaque monkey. NeuroImage14:S27–S32.

61. Matelli, M., G. Luppino, and G. Rizzolatti. 1985. Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav. Brain Res. 18:125–136.

62. Matelli, M., G. Luppino, and G. Rizzolatti. 1991. Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J. Comp. Neurol. 311:445–462.

63. Moll, L., and H. G. Kuypers. 1977. Premotor cortical ablations in monkeys: contralateral changes in visually guided reaching behavior.Science 198:317–319.

64. Monaco, S., C. Cavina-Pratesi, A. Sedda, P. Fattori, C. Galletti, and J. C. Culham. 2011. Functional magnetic resonance adaptation reveals the involvement of the dorsomedial stream in hand orientation for grasping. J. Neurophysiol. 106:2248–2263.

65. Monaco, S., A. Sedda, C. Cavina-Pratesi, and J. C. Culham. 2015. Neural correlates of object size and object location during grasping actions. Eur. J. Neurosci. 41:454–465.

66. Muir, R. B., and R. N. Lemon. 1983. Corticospinal neurons with a special role in precision grip. Brain Res. 261:312–316.

67. Murata, A., L. Fadiga, L. Fogassi, V. Gallese, V. Raos, and G. Rizzolatti. 1997. Object representation in the ventral premotor cortex (area F5) of the monkey. J. Neurophysiol. 78:2226–2230.

68. Murata, A., V. Gallese, G. Luppino, M. Kaseda, and H. Sakata. 2000. Selectivity for the shape, size and orientation of objects for grasping in neurons of monkey parietal area AIP. J. Neurophysiol. 83:2580–2601.

69. Oldfield, R. C. 1971. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9:97–113.

70. O'Toole, A. J., F. Jiang, H. Abdi, N. Pénard, J. P. Dunlop, and M. A. Parent. 2007. Theoretical, statistical, and practical perspectives on pattern-based classification approaches to the analysis of functional neuroimaging data. J. Cogn. Neurosci. 19:1735–1752.

71. Passingham, R. E. 1987. Two cortical systems for directing movement. Ciba Found. Symp. 132:151–164.

72. Pereira, F., T. Mitchell, and M. Botvinick. 2009. Machine learning classifiers and fMRI: a tutorial overview. NeuroImage 45:S199–S209.

73. Pitzalis, S., M. I. Sereno, G. Committeri, P. Fattori, G. Galati, A. Tosoni, et al. 2013. The human homologue of macaque area V6A.NeuroImage 82:517–530.

74. Pitzalis, S., P. Fattori, and C. Galletti. 2015. The human cortical areas V6 and V6A. Vis. Neurosci. 32:E007.

75. Prado, J., S. Clavagnier, H. Otzenberger, C. Scheiber, H. Kennedy, and M. T. Perenin. 2005. Two cortical systems for reaching in central and peripheral vision. Neuron 48:849–858.

76. Raos, V., M. A. Umilta, V. Gallese, and L. Fogassi. 2004. Functional properties of grasping-related neurons in the dorsal premotor area F2 of the macaque monkey. J. Neurophysiol. 92:1990–2002.

77. Raos, V., M. A. Umiltà, A. Murata, L. Fogassi, and V. Gallese. 2006. Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. J. Neurophysiol. 95:709–729.

78. Rice, N. J., E. Tunik, and S. T. Grafton. 2006. The anterior intraparietal sulcus mediates grasp execution, independent of requirement to update: new insights from transcranial magnetic stimulation. J. Neurosci. 26:8176–8182.

79. Rizzolatti, G., and M. A. Arbib. 1998. Language within our grasp. Trends Neurosci. 21:188–194.

80. Rizzolatti, G., and G. Luppino. 2001. The cortical motor system. Neuron 31:889–901.

81. Rizzolatti, G., L. Camarda, L. Fogassi, M. Gentilucci, G. Luppino, and M. Matelli. 1988. Functional organization of inferior area 6 in the macaque monkey. Exp. Brain Res. 71:491–507.

82. Rizzolatti, G., G. Luppino, and M. Matelli. 1998. The organisation of the cortical motor system: new concepts. Electroencephalogr. Clin. Neurophysiol. 106:283–296.

83. Rizzolatti, G., L. Fogassi, and V. Gallese. 2002. Motor and cognitive functions of the ventral premotor cortex. Curr. Opin. Neurobiol.12:149–154.

84. Sartori, L., E. Straulino, and U. Castiello. 2011. How objects are grasped: the interplay between affordances and end-goals. PLoS One6:e25203.

85. Scheperjans, F., K. Hermann, S. B. Eickhoff, K. Amunts, A. Schleicher, and K. Zilles. 2008. Observer-independent cytoarchitectonic mapping of the human superior parietal cortex. Cereb. Cortex 18:846–867.

86. Stelzer, J., G. Lohmann, K. Mueller, T. Buschmann, and R. Turner. 2014. Deficient approaches to human neuroimaging. Front. Hum. Neurosci. 8:462.

87. Taira, M., S. Mine, A. P. Georgopoulos, A. Murata, and H. Sakata. 1990. Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp. Brain Res. 83:29–36.

88. Tarantino, V., T. De Sanctis, E. Straulino, C. Begliomini, and U. Castiello. 2014. Object size modulates fronto-parietal activity during reaching movements. Eur. J. Neurosci. 39:1528–1537.

89. Tosoni, A., S. Pitzalis, G. Committeri, P. Fattori, C. Galletti, and G. Galati. 2014. Resting-state connectivity and functional specialization in human medial parieto-occipital cortex. Brain Struct. Funct. 220:3307–3321.

90. Tunik, E., S. H. Frey, and S. T. Grafton. 2005. Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustment of grasp. Nat. Neurosci. 8:505–511.

91. Tunik, E., N. J. Rice, A. Hamilton, and S. T. Grafton. 2007. Beyond grasping: representation of action in human anterior intraparietal sulcus. NeuroImage 36:T77–T86.

92. Vesia, M., and J. D. Crawford. 2012. Specialization of reach function in human posterior parietal cortex. Exp Brain Res. 221:1-18.

93. Weinrich, M., and S. P. Wise. 1982. The premotor cortex of the monkey. J. Neurosci. 2:1329–1345.

94. Xia, M., J. Wang, and Y. He. 2013. BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One 8:e68910.

95. Zorzi, M., M. G. Di Bono, and W. Fias. 2011. Distinct representations of numerical and non-numerical order in the human intraparietal sulcus revealed by multivariate pattern recognition. NeuroImage 56:674–680.