1932

Abstract

Humans and other primates possess a unique capacity to grasp and manipulate objects skillfully, a facility pervasive in everyday life that has undoubtedly contributed to the success of our species. When we reach and grasp an object, various cortical areas in the parietal and frontal lobes work together effortlessly to analyze object shape and position, transform this visual information into useful motor commands, and implement these motor representations to preshape the hand before contact with the object is made. In recent years, a growing number of studies have investigated the neural circuits underlying object grasping in both the visual and motor systems of the macaque monkey. The accumulated knowledge not only helps researchers understand how object grasping is implemented in the primate brain but may also contribute to the development of novel neural interfaces and neuroprosthetics.

Associated Article

There are media items related to this article:
Visual Guidance in Control of Grasping: Supplemental Video 1
Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-071714-034028
2015-07-08
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/neuro/38/1/annurev-neuro-071714-034028.html?itemId=/content/journals/10.1146/annurev-neuro-071714-034028&mimeType=html&fmt=ahah

Literature Cited

  1. Aggarwal V, Mollazadeh M, Davidson AG, Schieber MH, Thakor NV. 2013. State-based decoding of hand and finger kinematics using neuronal ensemble and LFP activity during dexterous reach-to-grasp movements. J. Neurophysiol. 109:3067–81 [Google Scholar]
  2. Andersen RA, Snyder LH, Bradley DC, Xing J. 1997. Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu. Rev. Neurosci. 20:303–30 [Google Scholar]
  3. Asher I, Stark E, Abeles M, Prut Y. 2007. Comparison of direction and object selectivity of local field potentials and single units in macaque posterior parietal cortex during prehension. J. Neurophysiol. 97:3684–95 [Google Scholar]
  4. Barrese JC, Rao N, Paroo K, Triebwasser C, Vargas-Irwin C. et al. 2013. Failure mode analysis of silicon-based intracortical microelectrode arrays in non-human primates. J. Neural Eng. 10:066014 [Google Scholar]
  5. Baumann MA, Fluet MC, Scherberger H. 2009. Context-specific grasp movement representation in the macaque anterior intraparietal area. J. Neurosci. 29:6436–48 [Google Scholar]
  6. Belmalih A, Borra E, Contini M, Gerbella M, Rozzi S, Luppino G. 2009. Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex. J. Comp. Neurol. 512:183–217 [Google Scholar]
  7. Binkofski F, Dohle C, Posse S, Stephan KM, Hefter H. et al. 1998. Human anterior intraparietal area subserves prehension: a combined lesion and functional MRI activation study. Neurology 50:1253–59 [Google Scholar]
  8. Bonini L, Ugolotti Serventi F, Bruni S, Maranesi M, Bimbi M. et al. 2012. Selectivity for grip type and action goal in macaque inferior parietal and ventral premotor grasping neurons. J. Neurophysiol. 108:1607–19 [Google Scholar]
  9. Borra E, Belmalih A, Calzavara R, Gerbella M, Murata A. et al. 2008. Cortical connections of the macaque anterior intraparietal (AIP) area. Cereb. Cortex 18:1094–111 [Google Scholar]
  10. Boudreau MJ, Brochier T, Pare M, Smith AM. 2001. Activity in ventral and dorsal premotor cortex in response to predictable force-pulse perturbations in a precision grip task. J. Neurophysiol. 86:1067–78 [Google Scholar]
  11. Carpaneto J, Umilta MA, Fogassi L, Murata A, Gallese V. et al. 2011. Decoding the activity of grasping neurons recorded from the ventral premotor area F5 of the macaque monkey. Neuroscience 188:80–94 [Google Scholar]
  12. Cisek P, Kalaska JF. 2002. Simultaneous encoding of multiple potential reach directions in dorsal premotor cortex. J. Neurophysiol. 87:1149–54 [Google Scholar]
  13. Cisek P, Kalaska JF. 2005. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45:801–14 [Google Scholar]
  14. Cisek P, Kalaska JF. 2010. Neural mechanisms for interacting with a world full of action choices. Annu. Rev. Neurosci. 33:269–98 [Google Scholar]
  15. Coe B, Tomihara K, Matsuzawa M, Hikosaka O. 2002. Visual and anticipatory bias in three cortical eye fields of the monkey during an adaptive decision-making task. J. Neurosci. 22:5081–90 [Google Scholar]
  16. Collinger JL, Wodlinger B, Downey JE, Wang W, Tyler-Kabara EC. et al. 2013. High-performance neuroprosthetic control by an individual with tetraplegia. Lancet 381:557–64 [Google Scholar]
  17. Cos I, Belanger N, Cisek P. 2011. The influence of predicted arm biomechanics on decision making. J. Neurophysiol. 105:3022–33 [Google Scholar]
  18. Cui H, Andersen RA. 2007. Posterior parietal cortex encodes autonomously selected motor plans. Neuron 56:552–59 [Google Scholar]
  19. Culham JC, Valyear KF. 2006. Human parietal cortex in action. Curr. Opin. Neurobiol. 16:205–12 [Google Scholar]
  20. Durand JB, Nelissen K, Joly O, Wardak C, Todd JT. et al. 2007. Anterior regions of monkey parietal cortex process visual 3D shape. Neuron 55:493–505 [Google Scholar]
  21. Durand JB, Peeters R, Norman JF, Todd JT, Orban GA. 2009. Parietal regions processing visual 3D shape extracted from disparity. NeuroImage 46:1114–26 [Google Scholar]
  22. Fattori P, Breveglieri R, Raos V, Bosco A, Galletti C. 2012. Vision for action in the macaque medial posterior parietal cortex. J. Neurosci. 32:3221–34 [Google Scholar]
  23. Fattori P, Raos V, Breveglieri R, Bosco A, Marzocchi N, Galletti C. 2010. The dorsomedial pathway is not just for reaching: grasping neurons in the medial parieto-occipital cortex of the macaque monkey. J. Neurosci. 30:342–49 [Google Scholar]
  24. Fluet MC, Baumann MA, Scherberger H. 2010. Context-specific grasp movement representation in macaque ventral premotor cortex. J. Neurosci. 30:15175–84 [Google Scholar]
  25. Fogassi L, Gallese V, Buccino G, Craighero L, Fadiga L, Rizzolatti G. 2001. Cortical mechanism for the visual guidance of hand grasping movements in the monkey: a reversible inactivation study. Brain 124:571–86 [Google Scholar]
  26. Gallese V, Murata A, Kaseda M, Niki N, Sakata H. 1994. Deficit of hand preshaping after muscimol injection in monkey parietal cortex. NeuroReport 5:1525–29 [Google Scholar]
  27. Galletti C, Kutz DF, Gamberini M, Breveglieri R, Fattori P. 2003. Role of the medial parieto-occipital cortex in the control of reaching and grasping movements. Exp. Brain Res. 153:158–70 [Google Scholar]
  28. Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G. 2011. Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5. Brain Struct. Funct. 216:43–65 [Google Scholar]
  29. Goodale MA, Milner AD. 1992. Separate visual pathways for perception and action. Trends Neurosci. 15:20–25 [Google Scholar]
  30. Grefkes C, Fink GR. 2005. The functional organization of the intraparietal sulcus in humans and monkeys. J. Anat. 207:3–17 [Google Scholar]
  31. Grefkes C, Weiss PH, Zilles K, Fink GR. 2002. Crossmodal processing of object features in human anterior intraparietal cortex: An fMRI study implies equivalencies between humans and monkeys. Neuron 35:173–84 [Google Scholar]
  32. Guipponi O, Wardak C, Ibarrola D, Comte JC, Sappey-Marinier D. et al. 2013. Multimodal convergence within the intraparietal sulcus of the macaque monkey. J. Neurosci. 33:4128–39 [Google Scholar]
  33. Hepp-Reymond MC, Hüsler EJ, Maier MA, Qi HX. 1994. Force-related neuronal activity in two regions of the primate ventral premotor cortex. Can. J. Physiol. Pharmacol. 72:571–79 [Google Scholar]
  34. Hepp-Reymond MC, Kirkpatrick-Tanner M, Gabernet L, Qi HX, Weber B. 1999. Context-dependent force coding in motor and premotor cortical areas. Exp. Brain Res. 128:123–33 [Google Scholar]
  35. Hochberg LR, Bacher D, Jarosiewicz B, Masse NY, Simeral JD. et al. 2012. Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 485:372–75 [Google Scholar]
  36. Hochberg LR, Serruya MD, Friehs GM, Mukand JA, Saleh M. et al. 2006. Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442:164–71 [Google Scholar]
  37. James TW, Culham J, Humphrey GK, Milner AD, Goodale MA. 2003. Ventral occipital lesions impair object recognition but not object-directed grasping: an fMRI study. Brain 126:2463–75 [Google Scholar]
  38. Janssen P, Vogels R, Liu Y, Orban GA. 2001. Macaque inferior temporal neurons are selective for three-dimensional boundaries and surfaces. J. Neurosci. 21:9419–29 [Google Scholar]
  39. Janssen P, Vogels R, Liu Y, Orban GA. 2003. At least at the level of inferior temporal cortex, the stereo correspondence problem is solved. Neuron 37:693–701 [Google Scholar]
  40. Janssen P, Vogels R, Orban GA. 1999. Macaque inferior temporal neurons are selective for disparity-defined three-dimensional shapes. PNAS 96:8217–22 [Google Scholar]
  41. Janssen P, Vogels R, Orban GA. 2000a. Selectivity for 3D shape that reveals distinct areas within macaque inferior temporal cortex. Science 288:2054–56 [Google Scholar]
  42. Janssen P, Vogels R, Orban GA. 2000b. Three-dimensional shape coding in inferior temporal cortex. Neuron 27:385–97 [Google Scholar]
  43. Jeannerod M. 1988. The Neural and Behavioral Organization of Goal-Directed Movements Oxford, UK: Oxford Univ. Press
  44. Jeannerod M, Biguer B. 1982. Visuomotor mechanisms in reaching within extrapersonal space. Analysis of Visual Behavior DJ Ingle, MA Goodale, RJW Mansfield 387–409 Cambridge, MA: MIT Press [Google Scholar]
  45. Jeannerod M, Decety J, Michel F. 1994. Impairment of grasping movements following a bilateral posterior parietal lesion. Neuropsychologia 32:369–80 [Google Scholar]
  46. Joly O, Vanduffel W, Orban GA. 2009. The monkey ventral premotor cortex processes 3D shape from disparity. NeuroImage 47:262–72 [Google Scholar]
  47. Klaes C, Westendorff S, Chakrabarti S, Gail A. 2011. Choosing goals, not rules: deciding among rule-based action plans. Neuron 70:536–48 [Google Scholar]
  48. Krug K, Cumming BG, Parker AJ. 2004. Comparing perceptual signals of single V5/MT neurons in two binocular depth tasks. J. Neurophysiol. 92:1586–96 [Google Scholar]
  49. Kuiken TA, Li G, Lock BA, Lipschutz RD, Miller LA. et al. 2009. Targeted muscle reinnervation for real-time myoelectric control of multifunction artificial arms. JAMA 301:619–28 [Google Scholar]
  50. Kurata K, Tanji J. 1986. Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J. Neurosci. 6:403–11 [Google Scholar]
  51. Lehmann SJ, Scherberger H. 2013. Reach and gaze representations in macaque parietal and premotor grasp areas. J. Neurosci. 33:7038–49 [Google Scholar]
  52. Lewis JW, Van Essen DC. 2000. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428:112–37 [Google Scholar]
  53. Luppino G, Murata A, Govoni P, Matelli M. 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. 128:181–87 [Google Scholar]
  54. Luppino G, Rizzolatti G. 2000. The organization of the frontal motor cortex. News Physiol. Sci. 15:219–24 [Google Scholar]
  55. Macaluso E, Driver J. 2001. Spatial attention and crossmodal interactions between vision and touch. Neuropsychologia 39:1304–16 [Google Scholar]
  56. McCoy AN, Platt ML. 2005. Expectations and outcomes: decision-making in the primate brain. J. Comp. Physiol. A 191:201–11 [Google Scholar]
  57. Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C. 1975. Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J. Neurophysiol. 38:871–908 [Google Scholar]
  58. Murata A, Fadiga L, Fogassi L, Gallese V, Raos V, Rizzolatti G. 1997. Object representation in the ventral premotor cortex (area F5) of the monkey. J. Neurophysiol. 78:2226–30 [Google Scholar]
  59. Murata A, Gallese V, Kaseda M, Sakata H. 1996. Parietal neurons related to memory-guided hand manipulation. J. Neurophysiol. 75:2180–86 [Google Scholar]
  60. Murata A, Gallese V, Luppino G, Kaseda M, Sakata H. 2000. Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. J. Neurophysiol. 83:2580–601 [Google Scholar]
  61. Musallam S, Corneil BD, Greger B, Scherberger H, Andersen RA. 2004. Cognitive control signals for neural prosthetics. Science 305:258–62 [Google Scholar]
  62. Nelissen K, Joly O, Durand JB, Todd JT, Vanduffel W, Orban GA. 2009. The extraction of depth structure from shading and texture in the macaque brain. PLOS ONE 4:e8306 [Google Scholar]
  63. Pani P, Theys T, Romero MC, Janssen P. 2014. Grasping execution and grasping observation activity of single neurons in the macaque anterior intraparietal area. J. Cogn. Neurosci. 26:2342–55 [Google Scholar]
  64. Pesaran B, Nelson MJ, Andersen RA. 2008. Free choice activates a decision circuit between frontal and parietal cortex. Nature 453:406–9 [Google Scholar]
  65. Premereur E, Van Dromme IC, Romero MC, Vanduffel W, Janssen P. 2015. Effective connectivity of depth structure–selective patches in the lateral bank of the macaque intraparietal sulcus. PLOS Biol. 13:e1002072 [Google Scholar]
  66. Raos V, Umilta MA, Murata A, Fogassi L, Gallese V. 2006. Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. J. Neurophysiol. 95:709–29 [Google Scholar]
  67. Rishel CA, Huang G, Freedman DJ. 2013. Independent category and spatial encoding in parietal cortex. Neuron 77:969–79 [Google Scholar]
  68. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M. 1988. Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp. Brain Res. 71:491–507 [Google Scholar]
  69. Rizzolatti G, Luppino G. 2001. The cortical motor system. Neuron 31:889–901 [Google Scholar]
  70. Romero MC, Pani P, Janssen P. 2014. Coding of shape features in the macaque anterior intraparietal area. J. Neurosci. 34:4006–21 [Google Scholar]
  71. Romero MC, Van Dromme IC, Janssen P. 2012. Responses to two-dimensional shapes in the macaque anterior intraparietal area. Eur. J. Neurosci. 36:2324–34 [Google Scholar]
  72. Romero MC, Van Dromme IC, Janssen P. 2013. The role of binocular disparity in stereoscopic images of objects in the macaque anterior intraparietal area. PLOS ONE 8:e55340 [Google Scholar]
  73. Sakata H, Taira M, Kusunoki M, Murata A, Tsutsui K. et al. 1999. Neural representation of three-dimensional features of manipulation objects with stereopsis. Exp. Brain Res. 128:160–69 [Google Scholar]
  74. Sakata H, Taira M, Murata A, Mine S. 1995. Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. Cereb. Cortex 5:429–38 [Google Scholar]
  75. Santhanam G, Ryu SI, Yu BM, Afshar A, Shenoy KV. 2006. A high-performance brain-computer interface. Nature 442:195–98 [Google Scholar]
  76. Schaffelhofer S, Agudelo-Toro A, Scherberger H. 2015. Decoding a wide range of hand configurations from macaque motor, premotor, and parietal cortex. J. Neurosci. 35:1068–81 [Google Scholar]
  77. Schaffelhofer S, Scherberger H. 2012. A new method of accurate hand- and arm-tracking for small primates. J. Neural Eng. 9:026025 [Google Scholar]
  78. Scherberger H, Andersen RA. 2007. Target selection signals for arm reaching in the posterior parietal cortex. J. Neurosci. 27:2001–12 [Google Scholar]
  79. Shadlen MN, Newsome WT. 2001. Neural basis of a perceptual decision in the parietal cortex (area lip) of the rhesus monkey. J. Neurophysiol. 86:1916–36 [Google Scholar]
  80. Shimazu H, Maier MA, Cerri G, Kirkwood PA, Lemon RN. 2004. Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. J. Neurosci. 24:1200–11 [Google Scholar]
  81. Srivastava S, Orban GA, De Maziere PA, Janssen P. 2009. A distinct representation of three-dimensional shape in macaque anterior intraparietal area: fast, metric, and coarse. J. Neurosci. 29:10613–26 [Google Scholar]
  82. Stark E, Asher I, Abeles M. 2007. Encoding of reach and grasp by single neurons in premotor cortex is independent of recording site. J. Neurophysiol. 97:3351–64 [Google Scholar]
  83. Subasi E, Townsend B, Scherberger H. 2010. In search of more robust decoding algorithms for neural prostheses, a data driven approach. Proc. 32nd Annu. Int. Conf. IEEE Eng. Med. Biol. Soc., Buenos Aires, Argent., Aug. 31–Sept. 44172–75
  84. Sugrue LP, Corrado GS, Newsome WT. 2004. Matching behavior and the representation of value in the parietal cortex. Science 304:1782–87 [Google Scholar]
  85. Taira M, Mine S, Georgopoulos AP, Murata A, Sakata H. 1990. Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp. Brain Res. 83:29–36 [Google Scholar]
  86. Takemura A, Inoue Y, Kawano K, Quaia C, Miles FA. 2001. Single-unit activity in cortical area MST associated with disparity-vergence eye movements: evidence for population coding. J. Neurophysiol. 85:2245–66 [Google Scholar]
  87. Tanaka K. 1996. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19:109–39 [Google Scholar]
  88. Tanne J, Boussaoud D, Boyer-Zeller N, Rouiller EM. 1995. Direct visual pathways for reaching movements in the macaque monkey. NeuroReport 7:267–72 [Google Scholar]
  89. Tanne-Gariepy J, Rouiller EM, Boussaoud D. 2002. Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways. Exp. Brain Res. 145:91–103 [Google Scholar]
  90. Taylor DM, Tillery SI, Schwartz AB. 2002. Direct cortical control of 3D neuroprosthetic devices. Science 296:1829–32 [Google Scholar]
  91. Theys T, Pani P, van Loon J, Goffin J, Janssen P. 2012a. Selectivity for three-dimensional shape and grasping-related activity in the macaque ventral premotor cortex. J. Neurosci. 32:12038–50 [Google Scholar]
  92. Theys T, Pani P, van Loon J, Goffin J, Janssen P. 2013. Three-dimensional shape coding in grasping circuits: a comparison between the anterior intraparietal area and ventral premotor area F5a. J. Cogn. Neurosci. 25:352–64 [Google Scholar]
  93. Theys T, Srivastava S, van Loon J, Goffin J, Janssen P. 2012b. Selectivity for three-dimensional contours and surfaces in the anterior intraparietal area. J. Neurophysiol. 107:995–1008 [Google Scholar]
  94. Thompson KG, Hanes DP, Bichot NP, Schall JD. 1996. Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. J. Neurophysiol. 76:4040–55 [Google Scholar]
  95. Townsend BR, Subasi E, Scherberger H. 2011. Grasp movement decoding from premotor and parietal cortex. J. Neurosci. 31:14386–98 [Google Scholar]
  96. Umilta MA, Kohler E, Gallese V, Fogassi L, Fadiga L. et al. 2001. I know what you are doing. A neurophysiological study. Neuron 31:155–65 [Google Scholar]
  97. Vargas-Irwin CE, Shakhnarovich G, Yadollahpour P, Mislow JM, Black MJ, Donoghue JP. 2010. Decoding complete reach and grasp actions from local primary motor cortex populations. J. Neurosci. 30:9659–69 [Google Scholar]
  98. Velliste M, Perel S, Spalding MC, Whitford AS, Schwartz AB. 2008. Cortical control of a prosthetic arm for self-feeding. Nature 453:1098–101 [Google Scholar]
  99. Verhoef BE, Michelet P, Vogels R, Janssen P. 2014. Choice-related activity in the anterior intraparietal area during 3-D structure categorization. J. Cogn. Neurosci. 271104–15
  100. Verhoef BE, Vogels R, Janssen P. 2010. Contribution of inferior temporal and posterior parietal activity to three-dimensional shape perception. Curr. Biol. 20:909–13 [Google Scholar]
  101. Verhoef BE, Vogels R, Janssen P. 2011. Synchronization between the end stages of the dorsal and the ventral visual stream. J. Neurophysiol. 105:2030–42 [Google Scholar]
  102. Wolpaw JR, McFarland DJ. 2004. Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. PNAS 101:17849–54 [Google Scholar]
  103. Wolpaw JR, Wolpaw EW. 2012. Brain–Computer Interfaces: Principles and Practice New York: Oxford Univ. Press
/content/journals/10.1146/annurev-neuro-071714-034028
Loading
/content/journals/10.1146/annurev-neuro-071714-034028
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error