Functional Magnetic Resonance Imaging Adaptation Reveals the Cortical Networks for Processing Grasp-Relevant Object Properties
Cerebral Cortex June
Functional Magnetic Resonance Imaging Adaptation Reveals the Cortical Networks for Processing Grasp-Relevant Object Properties
Simona Monaco 1 2 3
Ying Chen 1 2 3
W.P. Medendorp 0 2
J.D. Crawford 1 2 3 5 6
Katja Fiehler 2 4
Denise Y.P. Henriques 1 2 3 6
0 Radboud University Nijmegen, Donders Institute for Brain , Cognition and Behaviour, Nijmegen 6500HB , The Netherlands
1 Canadian Action and Perception Network (CAPnet)
2 The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions , please
3 York University, Centre for Vision Research , Toronto, ON , Canada
4 University of Giessen , Experimental Psychology, Giessen , Germany
5 Department of Biology, York University , Toronto, ON , Canada
6 Departments of Psychology, Kinesiology, Health Sciences, and Neuroscience Graduate Diploma Program, York University , Toronto, ON , Canada
Grasping behaviors require the selection of grasp-relevant object dimensions, independent of overall object size. Previous neuroimaging studies found that the intraparietal cortex processes object size, but it is unknown whether the graspable dimension (i.e., grasp axis between selected points on the object) or the overall size of objects triggers activation in that region. We used functional magnetic resonance imaging adaptation to investigate human brain areas involved in processing the grasp-relevant dimension of real 3-dimensional objects in grasping and viewing tasks. Trials consisted of 2 sequential stimuli in which the object's grasp-relevant dimension, its global size, or both were novel or repeated. We found that calcarine and extrastriate visual areas adapted to object size regardless of the grasp-relevant dimension during viewing tasks. In contrast, the superior parietal occipital cortex (SPOC) and lateral occipital complex of the left hemisphere adapted to the grasp-relevant dimension regardless of object size and task. Finally, the dorsal premotor cortex adapted to the grasp-relevant dimension in grasping, but not in viewing, tasks, suggesting that motor processing was complete at this stage. Taken together, our results provide a complete cortical circuit for progressive transformation of general object properties into grasp-related responses.
functional magnetic resonance imaging adaptation; grasping; grasp-relevant dimension; object size
Introduction
The properties of an object are processed not only based on
its physical appearance, like the surface and shape, but also
on the possible actions that it could afford depending on our
motor capabilities (Gibson 1979). For instance, if the intent is
to grasp an object, then the graspable dimension becomes
the most relevant property (Ganel and Goodale 2003). In fact,
planning a precision grip requires the selection of the grasp
axis on the object (distance between selected locations
for index finger and thumb), which will determine the grip
aperture. We will refer to this axis as the graspable or
grasp-relevant dimension of an object. Usually, an object
has several potential graspable dimensions that depend on
general object properties, and that become evident after a
quick initial analysis of the object. However, very little is
known about the cortical mechanisms that derive the
graspable dimension from more general object properties, and the
degree to which these processes might be separated at the
neural level is not yet understood.
Both primate electrophysiology and human neuroimaging
studies have implicated several cortical areas in coding object
properties, like size and shape. For example, it has been
shown that dorsal stream areas, such as the anterior
intraparietal area (AIP), process size, and shape of objects for
grasping actions (macaques: Murata et al. 2000; Asher et al. 2007;
Gardner et al. 2007; humans: Cavina-Pratesi et al. 2007;
Kroliczak et al. 2008; Chouinard et al. 2009; Monaco et al. 2010).
In addition, an area in the superior parietal occipital cortex of
humans (SPOC) and macaques (V6A) is involved in
processing and coordinating several components of grasping actions
(humans: Cavina-Pratesi et al. 2010; Gallivan et al. 2011,
Monaco et al. 2011; macaques: Fattori et al. 2009, 2010,
2012). Other areas in the intraparietal sulcus process object
size and shape during passive viewing, that is, irrespective of
a pending grasping movement (macaques: Sereno and
Maunsell 1998; Sereno et al. 2002; Sawamura et al. 2005; Lehky and
Sereno 2007; humans: Sawamura et al. 2005; Konen and
Kastner 2008; Monaco et al. 2010). Similarly, several human
imaging studies have shown that the lateral occipital complex
(LOC), a ventral stream area, is involved in processing object
properties for grasping movements (Culham et al. 2003; Singhal
et al. 2006; Monaco et al. 2010) as well as in viewing tasks (for
reviews see Grill-Spector et al. 2001; Kourtzi and Connor 2011).
Given the well-established involvement of the dorsal
stream in object-directed actions and the ventral s (...truncated)