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Experimental Brain Research

, Volume 112, Issue 1, pp 103–111 | Cite as

Localization of grasp representations in humans by positron emission tomography

2. Observation compared with imagination
  • Scott T. Grafton
  • Michael A. Arbib
  • Luciano Fadiga
  • Giacomo Rizzolatti
Research Article

Abstract

Positron emission tomography imaging of cerebral blood flow was used to localize brain areas involved in the representation of hand grasping movements. Seven normal subjects were scanned under three conditions. In the first, they observed precision grasping of common objects performed by the examiner. In the second, they imagined themselves grasping the objects without actually moving the hand. These two tasks were compared with a control task of object viewing. Grasp observation activated the left rostral superior temporal sulcus, left inferior frontal cortex (area 45), left rostral inferior parietal cortex (area 40), the rostral part of left supplementary motor area (SMA-proper), and the right dorsal premotor cortex. Imagined grasping activated the left inferior frontal (area 44) and middle frontal cortex, left caudal inferior parietal cortex (area 40), a more extensive response in left rostral SMA-proper, and left dorsal premotor cortex. The two conditions activated different areas of the right posterior cerebellar cortex. We propose that the areas active during grasping observation may form a circuit for recognition of hand-object interactions, whereas the areas active during imagined grasping may be a putative human homologue of a circuit for hand grasping movements recently defined in nonhuman primates. The location of responses in SMA-proper confirms the rostrocaudal segregation of this area for imagined and real movement. A similar segregation is also present in the cerebellum, with imagined and observed grasping movements activating different parts of the posterior lobe and real movements activating the anterior lobe.

Key words

Motor control Positron emission tomography Cerebral blood flow Grasp Imagined movements Human 

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References

  1. Arbib MA (1981) Perceptual structures and distributed motor control. In: Brooks VB (ed) Motor control (Handbook of physiology, sect 2, The nervous system, vol II, part 1) American Physiological Society, Bethesda, pp 1449–1480Google Scholar
  2. Bailey P, Bonin G von (1951) The isocortex of man. University of Illinois Press, UrbanaGoogle Scholar
  3. Bonda E, Petrides M, Frey S, Evans AC (1994) Frontal cortex involvement in organized sequences of hand movements: evidence from a positron emission tomography study. Soc Neurosci Abstr 20: 152.6Google Scholar
  4. Campbell AW (1905) Histological studies on the localization of cerebral function. Cambridge University Presss, New YorkGoogle Scholar
  5. Colebatch JG, Deiber M-P, Passingham RE, Friston KJ, Frackowiak RSJ (1991) Regional cerebral blood flow during voluntary arm and hand movements in human subjects. J Neurophysiol 65: 1392–1401Google Scholar
  6. Decety J, Sjoholm H, Ryding E, Stenberg G, Ingvar DH (1990) The cerebellum participates in mental activity: tomographic measurements. Brain Res 535: 313–317Google Scholar
  7. Decety J, Perani D, Jeannerod M, Bettinardi V, Tadary B, Woods R, Mazziotta JC, Fazio F (1994) Mapping motor representations with PET. Nature 371: 600–602Google Scholar
  8. Deiber M-P, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RSJ (1991) Cortical areas and the selection of movement: a study with PET. Exp Brain Res 84: 393–402Google Scholar
  9. Dum RP, Strick PL (1991) The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11: 667–689Google Scholar
  10. Economo C von (1929) The cytoarchitectonics of the human cerebral cortex. Oxford University Press, LondonGoogle Scholar
  11. Fox PT, Mintun MA, Raichle ME, Herscovitch P (1984) A non-invasive approach to quantitative functional brain mapping with H215O and positron emission tomography. J Cereb Blood Flow Metab 4: 329–333Google Scholar
  12. Friston KJ, Frith CD, Liddle PF, Frackowiak RSJ (1991) Comparing functional (PET) images: the assessement of significant change. J Cereb Blood Flow Metab 11: 690–699Google Scholar
  13. Fuster JM (1995) Memory in the cerebral cortex. MIT Press, CambridgeGoogle Scholar
  14. Gallese V, Murata A, Kaseda M, Niki N, Sakata H (1994) Deficit of hand preshaping after muscimol injection in monkey parietal cortex. Neuroreport 5: 1525–1529Google Scholar
  15. Gentilucci M, Fogassi L, Luppino G, Matelli M, Camarda R, Rizzolatti G (1988) Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements. Exp Brain Res 71: 475–490Google Scholar
  16. Godschalk M, Lemon RN, Kuypers HGJM, Ronday HK (1984) Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study. Exp Brain Res 56: 410–424Google Scholar
  17. Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Plum F, Mountcastle V (eds) Higher functions of the brain. (Handbook of physiology, sect 1, The nervous system, vol V) American Physiology Society, Bethesda, pp 373–417Google Scholar
  18. Grafton ST, Huang SC, Mahoney DK, Mazziotta JC, Phelps ME (1990) Analysis of optimal reconstruction filters for maximizing signal to noise ratios in PET cerebral blood flow studies (abstract). J Nucl Med 31: 865Google Scholar
  19. Grafton ST, Woods RP, Mazziotta JC, Phelps ME (1991) Somatotopic mapping of the primary motor cortex in man: activation studies with cerebral blood flow and PET. J Neurophysiol 66: 735–743Google Scholar
  20. Grafton ST, Mazziotta JC, Woods RP, Phelps ME (1992) Human functional anatomy of visually guided finger movements. Brain 115: 565–587Google Scholar
  21. Grafton ST, Woods RP, Tyszka JM (1994) Functional imaging of procedural motor learning: relating cerebral blood flow with individual subject performance. Hum Brain Mapp 1: 221–234Google Scholar
  22. Grafton ST, Fagg AH, Woods RP, Arbib MA (1996) Functional anatomy of pointing and grasping in humans. Cereb Cortex 6: 226–237Google Scholar
  23. Haxby JV, Grady CL, Horwitz B, Ungerleider LG, Mishkin M, Carson RE, Herscovitch P, Schapiro MB, Rapoport SI (1991) Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc Natl Acad Sci USA 88: 1621–1625Google Scholar
  24. He S-Q, Dum RP, Strick PL (1993) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci 13: 952–980Google Scholar
  25. He S-Q, Dum RP, Strick PL (1995) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci 15: 3284–3306Google Scholar
  26. Hepp-Reymond MC, Husler EJ, Maier MA, Qi HX (1994) Forcerelated neuronal activity in two regions fo the primate ventral premotor cortex. Can J Physiol Pharmacol 72: 571–579Google Scholar
  27. Herscovitch P, Markham J, Raichle ME (1983) Brain blood flow measured with intravenous H2 15O. I. Theory and error analysis. J Nucl Med 24: 782–789Google Scholar
  28. Jeannerod M (1988) The neural and behavioural organization of goal-directed movement. Oxford University Press, OxfordGoogle Scholar
  29. Jeannerod M (1994) The representing brain: neural correlates of motor intention and imagery. Behav Brain Sci 17: 187–245Google Scholar
  30. Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18: 314–320Google Scholar
  31. Jenkins IH, Brooks DJ, Nixon PD, Frackowiak RSJ, Passingham RE (1994) Motor sequence learning: a study with positron emission tomography. J Neurosci 14: 3775–3790Google Scholar
  32. Kimura D (1993) Neuromotor mechanisms in human communication. Oxford University Press, New YorkGoogle Scholar
  33. Kurata K (1993) Premotor cortex of monkeys: set- and movementrelated activity reflecting amplitude and direction of wrist movements. J Neurophysiol 69: 187–200Google Scholar
  34. Kurata K, Tanji J (1986) Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J Neurosci 6: 403–411Google Scholar
  35. Leinonen L, Nyman G (1979) Functional properties of cells in antero-lateral part of area 7 associative face area of awake monkeys. Exp Brain Res 34: 321–333Google Scholar
  36. Luppino G, Matelli M, Camarda RM, Gallese V, Rizzolatti G (1991) Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey. J Comp Neurol 311: 463–482Google Scholar
  37. Matelli M, Camarda M, Glickstein M, Rizzolatti G (1986) Afferent and efferent projections of the inferior area 6 in the macaque monkey. J Comp Neurol 251: 281–298Google Scholar
  38. Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and of adjacent cingulate cortex. J Comp Neurol 311: 445–462Google Scholar
  39. Matelli M, Rizzolatti G, Bettinardi V, Gilardi MC, Perani D, Rizzo G, Fazio F (1993) Activation of precentral and mesial motor areas during the execution of elementary proximal and distal arm movements: a PET study. Neuroreport 4: 1295–1298Google Scholar
  40. Matsumura M, Kubota K (1979) Cortical projections of hand-arm motor area from postarcuate area in macaque monkey: a histological study of retrograde transport of horse radish peroxidase. Neurosci Lett 11: 241–246Google Scholar
  41. Matsuzaka Y, Aizawa H, Tanji J (1992) A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. J Neurophysiol 68: 653–662Google Scholar
  42. Mazziotta JC, Huang S-C, Phelps ME, Carson RE, MacDonald NS, Mahoney K (1985) A noninvasive positron computed tomography technique using oxygen-15-labeled water for the evaluation of neurobehavioral task batteries. J Cereb Blood Flow Metab 5: 70–78Google Scholar
  43. Milner AD, Goodale MA (1995) The visual brain in action. Oxford University Press, OxfordGoogle Scholar
  44. Muakkassa KF, Strick PL (1994) Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized “premotor” areas. Brain Res 177: 176–182Google Scholar
  45. Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models. Irwin, BostonGoogle Scholar
  46. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97–113Google Scholar
  47. Orgogozo JM., Larsen B (1979) Activation of the supplementary motor area during voluntary movement in man suggests it works as a supramotor area. Science 206: 847–850Google Scholar
  48. Parsons LM, Fox PT, Downs JH, Glass T, Hirsch TB, Martin CC, Jerabek PA, Lancaster JL (1995) Use of implicit motor imagery for visual shape discrimination as revealed by PET. Nature 375: 54–56Google Scholar
  49. Passingham R (1993) The frontal lobes and voluntary action. Oxford University Press, OxfordGoogle Scholar
  50. Pellegrino G di, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp Brain Res 91: 176–180Google Scholar
  51. Perrett DI, Harries MH, Bevan R, Thomas S, Benson PJ, Mistlin AJ, Chitty AJ, Hietanen JK, Ortega JE (1989) Frameworks of analysis for the neural representation of animate objects and actions. J Exp Biol 146: 87–113Google Scholar
  52. Perrett DI, Mistlin AJ, Harries MH, Chitty AJ (1990) Understanding the visual appearance and consequence of hand actions. In: Goodale MA (ed) Vision and action: the control of grasping. Ablex, Norwood, NJ, pp 163–180Google Scholar
  53. Peterson SE, Fox PT, Posner MI, Mintun M, Raichle ME (1988) Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature 331: 585–589Google Scholar
  54. Petrides M, Pandya DN (1984) Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J Comp Neurol 228: 105–116Google Scholar
  55. Petrides M, Pandya DN (1994) Comparative architectonic analysis of the human and the macaque frontal cortex. In: Boiler F, Grafman J (ed) Handbook of neuropsychology. Elsevier, New York, pp 17–58Google Scholar
  56. Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex (in press)Google Scholar
  57. Raichle ME, Martin WRW, Herscovitch P (1983) Brain blood flow measured with intravenous HH215O. II. Implementation and validation. J Nucl Med 24: 790–798Google Scholar
  58. Rao SM, Binder JR, Bandettini PA, Hammeke TA, Yetkin FZ, Jesmanowicz A, Lisk LM, Morris GL, Mueller WM, Estkowski LD, Wong EC, Haughton VM, Hyde JS (1993) Functional magnetic resonance imaging of complex human movements. Neurology 43: 2311–2318Google Scholar
  59. Rizzolatti G, Scandolara C, Gentilucci G, Matelli M, Gentiluuci M (1981) Afferent properties of peri-arcuate neurons in macaque monkeys. II. Visual responses. Behav Brain Res 2: 147–163Google Scholar
  60. Rizzolatti GM, Gentilucci L, Fogassi G, Luppino G, Matelli M, Ponzoni-Maggi S (1987) Neurons related to goal-directed motor acts in inferior area 6 of the macaque monkey. Exp Brain Res 67: 220–224Google Scholar
  61. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkely. II. Area F5 and the control of distal movements. Exp Brain Res 71: 491–507Google Scholar
  62. Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996a) Premotor cortex and the recognition of motor actions. Cogn Brain Res 3: 131–141Google Scholar
  63. Rizzolatti G, Fadiga L, Matelli M, Bettinardi V, Perani D, Fazio F (1996b) Localization of grasp representations in humans by PET. 1. Observation versus execution. Exp Brain Res (in press)Google Scholar
  64. Roland PE, Larsen B, Lassen NA, Skinhøj E (1980) Supplementary motor area and other cortical areas in organization of voluntary movements in man. J Neurophysiology 43: 118–136Google Scholar
  65. Seltzer B, Pandya DN (1978) Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res 149: 106–109Google Scholar
  66. Sergent J, Zuck E, Terriah S, MacDonald B (1992) Distributed neural network underlying musical sight-reading and keyboard performance. Science 257: 106–109Google Scholar
  67. Stephan KM, Fink GR, Passingham RE, Silbersweig D, Ceballos-Baumann AO, Frith CD, Frackowiak RSJ (1995) Imaging the execution of movements. J Neurophysiol 73: 373–386Google Scholar
  68. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the brain. Thieme Medical, New YorkGoogle Scholar
  69. Tanji J (1994) The supplementary motor area in the cerebral cortex. Neurosci Res 19: 251–268Google Scholar
  70. Thach WT (1996) On the specific role of the cerebellum in motor learning and cognition: cluses from PET activation and lesion studies in man. Behav Brain SciGoogle Scholar
  71. Tyszka JM, Grafton ST, Chew W, Woods RP, Colletti PM (1994) Parcellation of mesial frontal motor areas during ideation and movement using functional magnetic resonance imaging at 1.5 Tesla. Ann Neurol 35: 746–749Google Scholar
  72. Watson JD, Myers R, Frackowiak RS, Hajnal JV, Woods RP, Mazziotta JC, Shipp S, Zeki S (1993) Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb Cortex 3: 79–94Google Scholar
  73. Webster MJ, Bachevalier J, Ungerleider LG (1994) Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb Cortex 4: 470–483Google Scholar
  74. Weisendanger M (1986) Recent developments in studies of the supplementary motor area of primates. Rev Physiol Biochem Pharmacol 103: 1–59Google Scholar
  75. Wise SP, Desimone R (1988) Behavioral neurophysiology: insights into seeing and grasping. Science 242: 736–741Google Scholar
  76. Woods RP, Cherry SR, Mazziotta JC (1992) Rapid automated algorithm for aligning and reslicing PET images. J Comp Assist Tomog 115: 565–587Google Scholar
  77. Woods RP, Mazziotta JC, Cherry SR (1993) Automated image registration. Ann Nucl Med [Suppl] 7: S70Google Scholar
  78. Woods RP, Iacoboni M, Grafton ST, Mazziotta JC (1996) Threeway analysis of variance. In: Myers R, Cunningham V, Bailey D (ed) Quantification of brain function using PET. Academic, New York, pp 353–358Google Scholar
  79. Worsley KJ, Evans AC, Marrett S, Neelin P (1992) A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab 12: 900–918Google Scholar
  80. Zatorre RJ, Evans AC, Meyer E, Gjedde A (1992) Lateralization of phonetic and pitch discrimination in speech processing. Science 256: 846–849Google Scholar
  81. Zilles K, Schlaug G, Geyger S, Luppino G, Matelli M, Qu M, Schormann T (1996) Anatomy and transmitter receptors of the supplementary motor areas in the human and non human primate brain. Adv Neurol 70: 29–43Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Scott T. Grafton
    • 1
  • Michael A. Arbib
    • 2
  • Luciano Fadiga
    • 3
  • Giacomo Rizzolatti
    • 3
  1. 1.The USC PET Imaging Sciences Center, Departments of Radiology and Neurology, University of Southern CaliforniaEos AngelesUSA
  2. 2.Center for Neural Engineering, University of Southern CaliforniaEos AngelesUSA
  3. 3.Istituto Di Fisiologia Umana, Universita Degli Studi Di ParmaItaly

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