Abstract
Although both reaching and grasping require transporting the hand to the object location, only grasping also requires processing of object shape, size and orientation to preshape the hand. Behavioural and neuropsychological evidence suggests that the object processing required for grasping relies on different neural substrates from those mediating object recognition. Specifically, whereas object recognition is believed to rely on structures in the ventral (occipitotemporal) stream, object grasping appears to rely on structures in the dorsal (occipitoparietal) stream. We used functional magnetic resonance imaging (fMRI) to determine whether grasping (compared to reaching) produced activation in dorsal areas, ventral areas, or both. We found greater activity for grasping than reaching in several regions, including anterior intraparietal (AIP) cortex. We also performed a standard object perception localizer (comparing intact vs. scrambled 2D object images) in the same subjects to identify the lateral occipital complex (LOC), a ventral stream area believed to play a critical role in object recognition. Although LOC was activated by the objects presented on both grasping and reaching trials, there was no greater activity for grasping compared to reaching. These results suggest that dorsal areas, including AIP, but not ventral areas such as LOC, play a fundamental role in computing object properties during grasping.
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Notes
Preliminary results from this study have previously appeared in abstract form (Culham et al. 2001).
References
Bandettini PA, Cox RW (2000) Event-related fMRI contrast when using constant interstimulus interval: theory and experiment. Magn Reson Med 43:540–548
Battaglini PP, Muzur A, Galletti C, Skrap M, Brovelli A, Fattori P (2002) Effects of lesions to area V6A in monkeys. Exp Brain Res 144:419–422
Binkofski F, Dohle C, Posse S, Stephan KM, Hefter H, Seitz RJ, Freund H-J (1998) Human anterior intraparietal area subserves prehension. Neurology 50:1253–1259
Binkofski F, Buccino G, Stephan KM, Rizzolatti G, Seitz RJ, Freund HJ (1999) A parieto-premotor network for object manipulation: evidence from neuroimaging. Exp Brain Res 128:210–213
Birn RM, Bandettini PA, Cox RW, Shaker R (1999) Event-related fMRI of tasks involving brief motion. Hum Brain Mapp 7:106–114
Bodegard A, Geyer S, Grefkes C, Zilles K, Roland PE (2001) Hierarchical processing of tactile shape in the human brain. Neuron 31:317–328
Chao LL, Martin A (2000) Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12:478–484
Connolly J, Andersen RA, Goodale MA (2003) fMRI evidence for a 'parietal reach region' in human brain. Exp Brain Res DOI 10.1007/s00221-003-1587-1
Culham J (in press) Human brain imaging reveals a parietal area specialized for grasping. In: Kanwisher N, Duncan J (eds) Attention and performance XX: functional neuroimaging of human cognition. Oxford University Press, Oxford
Culham JC, DeSouza JFX, Woodward S, Kourtzi Z, Gati JS, Menon RS, Goodale MA (2001) Visually-guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. J Vision 1:194
DeSouza JF, Dukelow SP, Gati JS, Menon RS, Andersen RA, Vilis T (2000) Eye position signal modulates a human parietal pointing region during memory-guided movements. J Neurosci 20:5835–5840
Ehrsson HH, Fagergren A, Jonsson T, Westling G, Johansson RS, Forssberg H (2000) Cortical activity in precision- versus power-grip tasks: an fMRI study. J Neurophysiol 83:528–536
Faillenot I, Sakata H, Costes N, Decety J, Jeannerod M (1997a) Visual working memory for shape and 3D-orientation: a PET study. Neuroreport 8:859–862
Faillenot I, Toni I, Decety J, Gregoire MC, Jeannerod M (1997b) Visual pathways for object-oriented action and object recognition: functional anatomy with PET. Cereb Cortex 7:77–85
Faillenot I, Decety J, Jeannerod M (1999) Human brain activity related to the perception of spatial features of objects. Neuroimage 10:114–124
Faillenot I, Sunaert S, Van Hecke P, Orban GA (2001) Orientation discrimination of objects and gratings compared: An fMRI study. Eur J Neurosci 13:585–596
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 124:571–586
Freire L, Mangin JF (2001) Motion correction algorithms may create spurious brain activations in the absence of subject motion. Neuroimage 14:709–722
Gallese V, Murata A, Kaseda M, Niki N, Sakata H (1994) Deficit of hand preshaping after muscimol injection in monkey parietal cortex. Neuroreport 5:1525–1529
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15:20–25
Goodale MA, Milner AD, Jakobson LS, Carey DP (1991) A neurological dissociation between perceiving objects and grasping them. Nature 349:154–156
Grafton ST, Fagg AH, Woods RP, Arbib MA (1996) Functional anatomy of pointing and grasping in humans. Cereb Cortex 6:226–237
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 35:173–184
Grill-Spector K, Kourtzi Z, Kanwisher N (2001) The lateral occipital complex and its role in object recognition. Vision Res 41:1409–1422
Jakobson LS, Archibald YM, Carey DP, Goodale MA (1991) A kinematic analysis of reaching and grasping movements in a patient recovering from optic ataxia. Neuropsychologia 29:803–809
James TW, Culham JC, Humphrey GK, Milner AD, Goodale MA (in press) fMRI evidence for a neurological dissociation between perceiving objects and grasping them. Brain
Jeannerod M (1981) Intersegmental coordination during reaching at natural visual objects. In: Long J, Baddeley A (eds) Attention and performance IX. Erlbaum, Hillsdale NJ, pp 153–168
Kawashima R, Naitoh E, Matsumura M, Itoh H, Ono S, Satoh K, Gotoh R, Koyama M, Inoue K, Yoshioka S, Fukuda H (1996) Topographic representation in human intraparietal sulcus of reaching and saccade. Neuroreport 7:1253–1256
Kinoshita H, Oku N, Hashikawa K, Nishimura T (2000) Functional brain areas used for the lifting of objects using a precision grip: a PET study. Brain Res 857:119–130
Kourtzi Z, Kanwisher N (2000) Cortical regions involved in perceiving object shape. J Neurosci 20:3310–3318
Kuhtz-Buschbeck JP, Ehrsson HH, Forssberg H (2001) Human brain activity in the control of fine static precision grip forces: an fMRI study. Eur J Neurosci 14:382–390
Lawrence BM, Snyder LH (2002) Effector specific and non-specific activity in frontal eye fields. Soc Neurosci Abstr:622.628
Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RBH (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci U S A 92:8135–8139
Malach R, Levy I, Hasson U (2002) The topography of high-order human object areas. Trends Cogn Sci 6:176–184
Matelli M, Camarda R, Glickstein M, Rizzolatti G (1986) Afferent and efferent projections of the inferior area 6 in the macaque monkey. J Comp Neurol 251:281–298
Matsumura M, Kawashima R, Naito E, Takahashi T, Satoh K, Yanagisawa T, Fukuda H (1996) Changes in rCBF during grasping in humans examined by PET. Neuroreport 7:749–752
Mecklinger A, Gruenewald C, Besson M, Magnie MN, Von Cramon DY (2002) Separable neuronal circuitries for manipulable and non-manipulable objects in working memory. Cereb Cortex 12:1115–1123
Muri RM, Iba-Zizen MT, Derosier C, Cabanis EA, Pierrot-Deseiligny C (1996) Location of the human posterior eye fields with functional magnetic resonance imaging. J Neurol Neurosurg Psychiatry 60:445–448
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh handedness inventory. Neuropsychologia 9:97–113
Rizzolatti G, Arbib MA (1998) Language within our grasp. Trends Neurosci 21:188–194
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
Rizzolatti G, Fadiga L, Matelli M, Bettinardi V, Paulesu E, Perani D, Fazio F (1996) Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp Brain Res 111:246–252
Roland PE, O'Sullivan B, Kawashima R (1998) Shape and roughness activate different somatosensory areas in the human brain. Proc Natl Acad Sci U S A 95:3295–3300
Sakata H, Taira M, Mine S, Murata A (1992) Hand-movement-related neurons of the posterior parietal cortex of the monkey: their role in the visual guidance of hand movements. In: Caminiti R, Johnson PB, Burnod Y (eds) Control of arm movement in space: neurophysiological and computational approaches. Springer, Heidelberg, pp 185–198
Sakata H, Taira M, Kusunoki M, Murata A, Tanaka Y (1997) The TINS lecture. The parietal association cortex in depth perception and visual control of hand action. Trends Neurosci 20:350–357
Sakata H, Taira M, Kusunoki M, Murata A, Tsutsui K, Tanaka Y, Shein WN, Miyashita Y (1999) Neural representation of three-dimensional features of manipulation objects with stereopsis. Exp Brain Res 128:160–169
Shikata E, Tanaka Y, Nakamura H, Taira M, Sakata H (1996) Selectivity of the parietal visual neurones in 3D orientation of surface of stereoscopic stimuli. Neuroreport 7:2389–2394
Shikata E, Hamzel F, Glauche V, Knab R, Dettmers C, Weiller C, Buchel C (2001) Surface orientation discrimination activates caudal and anterior intraparietal sulcus in humans: An event-related fMRI study. J Neurophysiol 85:1309–1314
Steeves JKE, Humphrey GK, Culham JC, Menon RS, Milner AD, Goodale MA (submitted) Behavioral and neuroimaging evidence for a contribution of color information to scene recognition in a patient with impaired form recognition
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
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical Publishers, New York
Wojciulik E, Kanwisher N (1999) The generality of parietal involvement in visual attention. Neuron 23:747–764
Acknowledgements
These projects would not have been possible without the engineering skills needed to design the apparatus. We are especially grateful to Dave Woytowich and Bob Stuart at UWO Engineering Machine Shops for designing and building the grasparatus, to Dan Pulham for wiring the electronics, to Leopold van Cleeff and Derek Quinlan for developing other hardware, and to Raynald Comtois for programming the input/output card. Philip Servos provided the air compressor and solenoids and assistance with their use. Zoe Kourtzi generously provided the object stimuli and Matlab code to present them. These experiments were supported by grants from the McDonnell-Pew Program in Cognitive Neuroscience (to JCC), the Canadian Institutes of Health Research (Operating Grant to MAG and NSERC/CIHR Multi-User Maintenance grant to RSM and colleagues), and the Canada Research Chairs Program (to MAG and RSM).
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Culham, J.C., Danckert, S.L., Souza, J.F.X.D. et al. Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res 153, 180–189 (2003). https://doi.org/10.1007/s00221-003-1591-5
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DOI: https://doi.org/10.1007/s00221-003-1591-5