Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-19T02:53:14.320Z Has data issue: false hasContentIssue false

The influence of complex action knowledge on representations of novel graspable objects: Evidence from functional magnetic resonance imaging

Published online by Cambridge University Press:  18 October 2007

SARAH H. CREEM-REGEHR
Affiliation:
Department of Psychology, University of Utah, Salt Lake City, Utah
VALENTINA DILDA
Affiliation:
Department of Psychology, University of Utah, Salt Lake City, Utah
APRIL E. VICCHRILLI
Affiliation:
Department of Psychology, University of Utah, Salt Lake City, Utah
FREDERICK FEDERER
Affiliation:
Graduate Program in Neuroscience, University of Utah, Salt Lake City, Utah
JAMES N. LEE
Affiliation:
Department of Radiology, University of Utah, Salt Lake City, Utah

Abstract

The influence of action knowledge associated with novel objects was investigated using functional magnetic resonance imaging. Participants were trained on complex actions associated with novel objects (“tools”) and had experience manipulating other visually similar novel objects (“shapes”). During scanning, participants viewed, imagined grasping, and imagined using the objects. Based on previous neuroimaging and neuropsychological findings, our primary goal was to examine frontal and parietal regions subserving action representations associated with visual objects, namely the left inferior parietal lobule (IPL), the left ventral premotor cortex (VPM) and the presupplementary motor cortex (pre-SMA). We predicted differences between the tool and shape stimuli, modulated also by task demands. In viewing, we found greater effect sizes in the left VPM and IPL for tools versus shapes. In grasping, there was similar activation with both object types. The largest differences existed in using, in which greater effect sizes were found for tools versus shapes in left IPL and pre-SMA, and marginally in the left VPM. We suggest that representations of tools extend beyond classically defined affordances and recruit processing about both graspability and known action plans in tasks involving visual memory, motor imagery, and motor execution. (JINS, 2007, 13, 1009–1020.)

Type
SYMPOSIA
Copyright
© 2007 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allport, D.A. (1985). Distributed memory, modular subsystems and dysphasia. In S.K. Newman & R. Epstein (Eds.), Current perspectives in dysphasia (pp. 3260). Edinburgh: Churchill Livingstone.
Beauchamp, M.S., Lee, K.E., Haxby, J.V., & Martin, A. (2002). Parallel visual motion processing streams for manipulable objects and human movements. Neuron, 34, 149159.CrossRefGoogle Scholar
Binkofski, F., Buccino, G., Stephan, K.M., Rizzolatti, G., Seitz, R.J., & Freund, H.-J. (1999). A parieto-premotor network for object manipulation: Evidence from neuroimaging. Experimental Brain Research, 128, 210213.CrossRefGoogle Scholar
Boronat, C., Buxbaum, L.J., Coslett, H.B., Tang, K., Saffran, E.M., Kimberg, D.Y., & Detre, J.A. (2005). Distinctions between function and manipulation knowledge of objects: Evidence from functional magnetic resonance imaging. Cognitive Brain Research, 23, 361473.Google Scholar
Brett, M., Anton, J., Valabreque, R., & Poline, J. (2002). Region of interest analysis using an SPM toolbox. Paper presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.
Buxbaum, L.J. (2001). Ideomotor apraxia: A call to action. Neurocase, 7, 445458.CrossRefGoogle Scholar
Buxbaum, L.J., Johnson-Frey, S.H., & Bartlett-Williams, M. (2005). Deficient internal models for planning hand-object interactions in apraxia. Neuropsychologia, 43, 917929.Google Scholar
Buxbaum, L.J., Kyle, K.M., Tang, K., & Detre, J.A. (2006). Neural substrates of knowledge of hand postures for object grasping and functional object use: Evidence from fMRI. Brain Research, 1117, 175185.Google Scholar
Buxbaum, L.J. & Saffran, E.M. (2002). Knowledge of object manipulation and object function: Dissociations in apraxic and non-apraxic subjects. Brain and Language, 82, 179199.Google Scholar
Buxbaum, L.J., Sirigu, A., Schwartz, M.F., & Klatzky, R.L. (2003). Cognitive representations of hand posture in ideomotor apraxia. Neuropsychologia, 41, 10911113.Google Scholar
Chao, L.L., Haxby, J.V., & Martin, A. (1999). Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neuroscience, 2, 913919.Google Scholar
Chao, L.L. & Martin, A. (2000). Representation of manipulable man-made objects in the dorsal stream. Neuroimage, 12, 478484.CrossRefGoogle Scholar
Choi, S.H., Na, D.L., Kang, E., Lee, K.M., Lee, S.W., & Na, D.G. (2001). Functional magnetic resonance imaging during pantomiming tool-use gestures. Experimental Brain Research, 139, 311317.CrossRefGoogle Scholar
Creem, S.H. & Proffitt, D.R. (1998). Two memories for geographical slant: Separation and interdependence of action and awareness. Psychonomic Bulletin and Review, 5, 2236.CrossRefGoogle Scholar
Creem-Regehr, S.H. & Lee, J.N. (2005). Neural representations of graspable objects: Are tools special? Cognitive Brain Research, 22, 457469.Google Scholar
Creem, S.H. & Proffitt, D.R. (2001a). Defining the cortical visual systems: “What”, “Where”, and “How”. Acta Psychologica, 107, 4368.Google Scholar
Creem, S.H. & Proffitt, D.R. (2001b). Grasping objects by their handles: A necessary interaction between cognition and action. Journal of Experimental Psychology: Human Perception and Performance, 27, 218228.Google Scholar
Culham, J.C., Danckert, S.L., De Souza, J.F.X., Gati, J.S., Menon, R.S., & Goodale, M.A. (2003). Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Experimental Brain Research, 153, 158170.Google Scholar
Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J.B., Frith, C.D., & Frackowiak, R.S.J. (1995). Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping, 2, 189210.Google Scholar
Gibson, J.J. (1979). The ecological approach to visual perception. Boston: Houghton Mifflin.
Glover, S. (2004). Separate visual representations in the planning and control of action. Behavioral and Brain Sciences, 27, 378.Google Scholar
Grezes, J. & Decety, J. (2001). Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta-analysis. Human Brain Mapping, 12, 119.Google Scholar
Grezes, J. & Decety, J. (2002). Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia, 40, 212222.Google Scholar
Grezes, J., Tucker, M., Armony, J.L., Ellis, R., & Passingham, R.E. (2003). Objects automatically potentiate action: An fMRI study of implicit processing. European Journal of Neuroscience, 17, 27352740.Google Scholar
Hanakawa, T., Immisch, I., Toma, K., Dimyan, M., Van Gelderen, P., & Hallett, M. (2003). Functional properties of brain areas associated with motor execution and imagery. Journal of Neurophysiology, 89, 9891002.Google Scholar
Imamizu, H., Kuroda, T., Miyauchi, S., Yoshioka, T., & Kawato, M. (2003). Modular organization of internal models of tools in the human cerebellum. Proceedings of the National Academy of Sciences United States of America, 100, 54615466.Google Scholar
Johnson-Frey, S.H. (2003). Cortical mechanisms of human tool use. In S.H. Johnson-Frey (Ed.), Taking action: Cognitive neuroscience perspectives on the problem of intentional acts (pp. 185217). Cambridge, MA: The MIT Press.
Johnson-Frey, S.H., Maloof, F.R., Newman-Norlund, R., Farrer, C., Inati, S., & Grafton, S.T. (2003). Actions or hand-object interactions? Human inferior frontal cortex and action observation. Neuron, 39, 10531058.Google Scholar
Johnson-Frey, S.H., Newman-Norlund, R., & Grafton, S.T. (2005). A distributed left hemisphere network active during planning of everyday tool use skills. Cerebral Cortex, 15, 681695.CrossRefGoogle Scholar
Johnson, S.H. & Grafton, S.T. (2003). From “acting on” to “acting with”: The functional anatomy of object-oriented action schemata. Progress in Brain Research, 142, 127139.Google Scholar
Lewis, J.W. (2006). Cortical networks related to human tool use. The Neuroscientist, 12, 211231.Google Scholar
Milner, A.D. & Goodale, M.A. (1995). The visual brain in action. Oxford: Oxford University Press.
Moll, J., de Oliveira-Souza, R., Passman, L.J., Cunha, F.C., Souza-Lima, F., & Andreiuolo, P.A. (2000). Functional MRI correlates of real and imagined tool-use pantomimes. Neurology, 54, 13311336.Google Scholar
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97113.CrossRefGoogle Scholar
Picard, N. & Strick, P.L. (2001). Imaging the premotor areas. Current Opinion in Neurobiology, 11, 663672.Google Scholar
Rizzolatti, G., Fogassi, L., & Gallese, V. (2002). Motor and cognitive functions of the ventral premotor cortex. Current Opinion in Neurobiology, 12, 149154.CrossRefGoogle Scholar
Rizzolatti, G. & Luppino, G. (2001). The cortical motor system. Neuron, 31, 889901.Google Scholar
Rizzolatti, G. & Matelli, M. (2003). Two different streams form the dorsal visual system: Anatomy and functions. Experimental Brain Research, 153, 146157.CrossRefGoogle Scholar
Rothi, L.J.G. & Heilman, K.M. (1997). Apraxia: The neuropsychology of action. Hove, UK: Psychology Press.
Rumiati, R.I., Weiss, P.H., Tessari, A., Assmus, A., Zilles, K., Herzog, H., & Fink, G.R. (2005). Common and differential neural mechanisms supporting imitation of meaningful and meaningless actions. Journal of Cognitive Neuroscience, 17, 14201431.CrossRefGoogle Scholar
Sakata, H. & Taira, M. (1994). Parietal control of hand action. Current Opinion in Neurobiology, 4, 847856.Google Scholar
Sirigu, A., Cohen, L., Duhamel, J., Pillon, B., Dubois, B., & Agid, Y. (1995). A selective impairment of hand posture for object utilization in apraxia. Cortex, 31, 4155.Google Scholar
Sirigu, A., Duhamel, J., Cohen, L., Pillon, B., Dubois, B., & Agid, Y. (1996). The mental representation of hand movements after parietal cortex damage. Science, 273, 15641568.Google Scholar
Tucker, M. & Ellis, R. (1998). On the relations between seen objects and components of potential actions. Journal of Experimental Psychology: Human Perception and Performance, 24, 830846.Google Scholar
Tucker, M. & Ellis, R. (2001). The potentiation of grasp types during visual object categorization. Visual Cognition, 8, 769800.CrossRefGoogle Scholar
Tucker, M. & Ellis, R. (2004). Action priming by briefly presented objects. Acta Psychologica, 116, 185203.Google Scholar
Warrington, E.K. & McCarthy, R.A. (1987). Categories of knowledge: Further fractionations and an attempted integration. Brain, 110, 12731296.CrossRefGoogle Scholar
Warrington, E.K. & Shallice, T. (1984). Category-specific semantic impairments. Brain, 107, 829853.CrossRefGoogle Scholar
Weisberg, J., van Turennout, M., & Martin, A. (2007). A neural system for learning about object function. Cerebral Cortex, 17, 513521.Google Scholar