Brain, Vol. 124, No. 3, 571-586,
March 2001
© 2001 Oxford University Press
Cortical mechanism for the visual guidance of hand grasping movements in the monkey
A reversible inactivation study
Istituto di Fisiologia Umana, Università di Parma, Italy
Correspondence to:
Leonardo Fogassi, Istituto di Fisologia Umana, Università di Parma, Via Volturno 39, I-43100 Parma, Italy E-mail: fogassi@unipr.it
Picking up an object requires two basic motor operations: reaching and grasping. Neurophysiological studies in monkeys have suggested that the visuomotor transformations necessary for these two operations are carried out by separate parietofrontal circuits and that, for grasping, a key role is played by a specific sector of the ventral premotor cortex: area F5. The aim of the present study was to test the validity of this hypothesis by reversibly inactivating area F5 in monkeys trained to grasp objects of different shape, size and orientation. In separate sessions, the hand field of the primary motor cortex (area F1 or area 4) was also reversibly inactivated. The results showed that after inactivation of area F5 buried in the bank of the arcuate sulcus (the F5 sector where visuomotor neurones responding to object presentation are located), the hand shaping preceding grasping was markedly impaired and the hand posture was not appropriate for the object size and shape. The monkeys were eventually able to grasp the objects, but only after a series of corrections made under tactile control. With small inactivations the deficits concerned the contralesional hand, with larger inactivations the ipsilateral hand as well. In addition, there were signs of peripersonal neglect in the hemispace contralateral to the inactivation site. Following inactivation of area F5 lying on the cortical convexity (the F5 sector where visuomotor neurones responding to action observation, `mirror neurones', are found) only a motor slowing was observed, the hand shaping being preserved. The inactivation of the hand field of area F1 produced a severe paralysis of contralateral finger movements with hypotonia. The results of this study indicate the crucial role of the ventral premotor cortex in visuomotor transformations for grasping movements. More generally, they provide strong support for the notion that distal and proximal movement organization relies upon distinct cortical circuits. Clinical data on distal movement deficits in humans are re-examined in the light of the present findings.
![]()
CiteULike
Connotea
Del.icio.us What's this?
This article has been cited by other articles:
![]() |
J. Majdandzic, H. Bekkering, H. T. van Schie, and I. Toni Movement-Specific Repetition Suppression in Ventral and Dorsal Premotor Cortex during Action Observation Cereb Cortex, November 1, 2009; 19(11): 2736 - 2745. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Nishimura and T. Isa Compensatory Changes at the Cerebral Cortical Level after Spinal Cord Injury Neuroscientist, October 1, 2009; 15(5): 436 - 444. [Abstract] [PDF] |
||||
![]() |
C. M. Hendrix, C. R. Mason, and T. J. Ebner Signaling of Grasp Dimension and Grasp Force in Dorsal Premotor Cortex and Primary Motor Cortex Neurons During Reach to Grasp in the Monkey J Neurophysiol, July 1, 2009; 102(1): 132 - 145. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. F. Balan and J. Gottlieb Functional Significance of Nonspatial Information in Monkey Lateral Intraparietal Area J. Neurosci., June 24, 2009; 29(25): 8166 - 8176. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Lingnau, B. Gesierich, and A. Caramazza Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans PNAS, June 16, 2009; 106(24): 9925 - 9930. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. L. Chen, V. B. Penhune, and R. J. Zatorre Listening to Musical Rhythms Recruits Motor Regions of the Brain Cereb Cortex, December 1, 2008; 18(12): 2844 - 2854. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. L. Pardo-Vazquez, V. Leboran, and C. Acuna Neural Correlates of Decisions and Their Outcomes in the Ventral Premotor Cortex J. Neurosci., November 19, 2008; 28(47): 12396 - 12408. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Kroliczak, T. D. McAdam, D. J. Quinlan, and J. C. Culham The Human Dorsal Stream Adapts to Real Actions and 3D Shape Processing: A Functional Magnetic Resonance Imaging Study J Neurophysiol, November 1, 2008; 100(5): 2627 - 2639. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Davare, R. Lemon, and E. Olivier Selective modulation of interactions between ventral premotor cortex and primary motor cortex during precision grasping in humans J. Physiol., June 1, 2008; 586(11): 2735 - 2742. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Borra, A. Belmalih, R. Calzavara, M. Gerbella, A. Murata, S. Rozzi, and G. Luppino Cortical Connections of the Macaque Anterior Intraparietal (AIP) Area Cereb Cortex, May 1, 2008; 18(5): 1094 - 1111. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Verhagen, H. C. Dijkerman, M. J. Grol, and I. Toni Perceptuo-Motor Interactions during Prehension Movements J. Neurosci., April 30, 2008; 28(18): 4726 - 4735. [Abstract] [Full Text] [PDF] |
||||
![]() |
U. Castiello and C. Begliomini The Cortical Control of Visually Guided Grasping Neuroscientist, April 1, 2008; 14(2): 157 - 170. [Abstract] [PDF] |
||||
![]() |
M. A. Umilta, L. Escola, I. Intskirveli, F. Grammont, M. Rochat, F. Caruana, A. Jezzini, V. Gallese, and G. Rizzolatti When pliers become fingers in the monkey motor system PNAS, February 12, 2008; 105(6): 2209 - 2213. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Sahin, M. Cakmak, M. R. Dogar, E. Ugur, and G. Ucoluk To Afford or Not to Afford: A New Formalization of Affordances Toward Affordance-Based Robot Control Adaptive Behavior, December 1, 2007; 15(4): 447 - 472. [Abstract] [PDF] |
||||
![]() |
M. J. Grol, J. Majdandzic, K. E. Stephan, L. Verhagen, H. C. Dijkerman, H. Bekkering, F. A. J. Verstraten, and I. Toni Parieto-Frontal Connectivity during Visually Guided Grasping J. Neurosci., October 31, 2007; 27(44): 11877 - 11887. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Tomassini, S. Jbabdi, J. C. Klein, T. E. J. Behrens, C. Pozzilli, P. M. Matthews, M. F. S. Rushworth, and H. Johansen-Berg Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Lateral Premotor Cortex Identifies Dorsal and Ventral Subregions with Anatomical and Functional Specializations J. Neurosci., September 19, 2007; 27(38): 10259 - 10269. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Pizzimenti, W. G. Darling, D. L. Rotella, D. W. McNeal, J. L. Herrick, J. Ge, K. S. Stilwell-Morecraft, and R. J. Morecraft Measurement of Reaching Kinematics and Prehensile Dexterity in Nonhuman Primates J Neurophysiol, August 1, 2007; 98(2): 1015 - 1029. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Umilta, T. Brochier, R. L. Spinks, and R. N. Lemon Simultaneous Recording of Macaque Premotor and Primary Motor Cortex Neuronal Populations Reveals Different Functional Contributions to Visuomotor Grasp J Neurophysiol, July 1, 2007; 98(1): 488 - 501. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Prabhu, M. Voss, T. Brochier, L. Cattaneo, P. Haggard, and R. Lemon Excitability of human motor cortex inputs prior to grasp J. Physiol., May 15, 2007; 581(1): 189 - 201. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Stark, I. Asher, and M. Abeles Encoding of Reach and Grasp by Single Neurons in Premotor Cortex Is Independent of Recording Site J Neurophysiol, May 1, 2007; 97(5): 3351 - 3364. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Davare, M. Andres, E. Clerget, J.-L. Thonnard, and E. Olivier Temporal Dissociation between Hand Shaping and Grip Force Scaling in the Anterior Intraparietal Area J. Neurosci., April 11, 2007; 27(15): 3974 - 3980. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. P. Gardner, J. Y. Ro, K. S. Babu, and S. Ghosh Neurophysiology of Prehension. II. Response Diversity in Primary Somatosensory (S-I) and Motor (M-I) Cortices J Neurophysiol, February 1, 2007; 97(2): 1656 - 1670. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. P. Gardner, K. S. Babu, S. D. Reitzen, S. Ghosh, A. S. Brown, J. Chen, A. L. Hall, M. D. Herzlinger, J. B. Kohlenstein, and J. Y. Ro Neurophysiology of Prehension. I. Posterior Parietal Cortex and Object-Oriented Hand Behaviors J Neurophysiol, January 1, 2007; 97(1): 387 - 406. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. J. Rice, E. Tunik, and S. T. Grafton The Anterior Intraparietal Sulcus Mediates Grasp Execution, Independent of Requirement to Update: New Insights from Transcranial Magnetic Stimulation J. Neurosci., August 2, 2006; 26(31): 8176 - 8182. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Hoshi and J. Tanji Differential Involvement of Neurons in the Dorsal and Ventral Premotor Cortex During Processing of Visual Signals for Action Planning J Neurophysiol, June 1, 2006; 95(6): 3596 - 3616. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Davare, M. Andres, G. Cosnard, J.-L. Thonnard, and E. Olivier Dissociating the role of ventral and dorsal premotor cortex in precision grasping. J. Neurosci., February 22, 2006; 26(8): 2260 - 2268. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Raos, M.-A. Umilta, A. Murata, L. Fogassi, and V. Gallese Functional Properties of Grasping-Related Neurons in the Ventral Premotor Area F5 of the Macaque Monkey J Neurophysiol, February 1, 2006; 95(2): 709 - 729. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Stefan, L. G. Cohen, J. Duque, R. Mazzocchio, P. Celnik, L. Sawaki, L. Ungerleider, and J. Classen Formation of a Motor Memory by Action Observation J. Neurosci., October 12, 2005; 25(41): 9339 - 9346. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Arunachalam, V. S. Weerasinghe, and K. R. Mills Motor Control of Rapid Sequential Finger Tapping in Humans J Neurophysiol, September 1, 2005; 94(3): 2162 - 2170. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. M. Friel, S. Barbay, S. B. Frost, E. J. Plautz, D. M. Hutchinson, A. M. Stowe, N. Dancause, E. V. Zoubina, B. M. Quaney, and R. J. Nudo Dissociation of Sensorimotor Deficits After Rostral Versus Caudal Lesions in the Primary Motor Cortex Hand Representation J Neurophysiol, August 1, 2005; 94(2): 1312 - 1324. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Ochiai, H. Mushiake, and J. Tanji Involvement of the Ventral Premotor Cortex in Controlling Image Motion of the Hand During Performance of a Target-capturing Task Cereb Cortex, July 1, 2005; 15(7): 929 - 937. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Cattaneo, M. Voss, T. Brochier, G. Prabhu, D. M. Wolpert, and R. N. Lemon A cortico-cortical mechanism mediating object-driven grasp in humans PNAS, January 18, 2005; 102(3): 898 - 903. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. A. Fridman, T. Hanakawa, M. Chung, F. Hummel, R. C. Leiguarda, and L. G. Cohen Reorganization of the human ipsilesional premotor cortex after stroke Brain, April 1, 2004; 127(4): 747 - 758. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Shimazu, M. A. Maier, G. Cerri, P. A. Kirkwood, and R. N. Lemon Macaque Ventral Premotor Cortex Exerts Powerful Facilitation of Motor Cortex Outputs to Upper Limb Motoneurons J. Neurosci., February 4, 2004; 24(5): 1200 - 1211. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. W. Krakauer, M.-F. Ghilardi, M. Mentis, A. Barnes, M. Veytsman, D. Eidelberg, and C. Ghez Differential Cortical and Subcortical Activations in Learning Rotations and Gains for Reaching: A PET Study J Neurophysiol, February 1, 2004; 91(2): 924 - 933. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Cerri, H. Shimazu, M. A. Maier, and R. N. Lemon Facilitation From Ventral Premotor Cortex of Primary Motor Cortex Outputs to Macaque Hand Muscles J Neurophysiol, August 1, 2003; 90(2): 832 - 842. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. B. Frost, S. Barbay, K. M. Friel, E. J. Plautz, and R. J. Nudo Reorganization of Remote Cortical Regions After Ischemic Brain Injury: A Potential Substrate for Stroke Recovery J Neurophysiol, June 1, 2003; 89(6): 3205 - 3214. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. C. Roy, Y. Paulignan, M. Meunier, and D. Boussaoud Prehension Movements in the Macaque Monkey: Effects of Object Size and Location J Neurophysiol, September 1, 2002; 88(3): 1491 - 1499. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. M. Galaburda, D. P. Holinger, U. Bellugi, and G. F. Sherman Williams Syndrome: Neuronal Size and Neuronal-Packing Density in Primary Visual Cortex Arch Neurol, September 1, 2002; 59(9): 1461 - 1467. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Hoshi and J. Tanji Contrasting Neuronal Activity in the Dorsal and Ventral Premotor Areas During Preparation to Reach J Neurophysiol, February 1, 2002; 87(2): 1123 - 1128. [Abstract] [Full Text] [PDF] |
||||








