Elsevier

NeuroImage

Volume 36, Supplement 2, 2007, Pages T94-T108
NeuroImage

Does tool-related fMRI activity within the intraparietal sulcus reflect the plan to grasp?

https://doi.org/10.1016/j.neuroimage.2007.03.031Get rights and content

Abstract

Neuroimaging investigations reliably describe a left-lateralized network of areas as underlying the representations of knowledge about familiar tools. Among the critical ‘nodes’ of the network, an area centered within the left intraparietal sulcus (IPS) is thought to be related to the motoric representations associated with familiar tools and their usage. This area is in the vicinity of an area implicated in the control of object-directed grasping actions: the anterior intraparietal area, AIP. The current study aimed to evaluate whether this tool-related intraparietal activity could be accounted for by the graspable nature of tools or whether it was due to additional factors such as the functionality of tools. First, we found that during a naming task activation within a discrete region of the left anterior intraparietal cortex was higher for tools than for graspable objects, but did not differ between graspable and non-graspable objects. In addition, the peak activity associated with tool naming was found to be largely distinct and consistently posterior to that associated with real object grasping. A separate region, anterior to the tool-selective focus and possibly overlapping with AIP, demonstrated weak selectivity for both tools and graspable objects relative to non-graspable objects.

These findings indicate that this tool-selective area at the anterior end of the left IPS is both separable from the grasp-related intraparietal activity and, consistently, it does not simply reflect the processing of grasping affordances. Taken together, these results suggest that object graspability alone cannot account for the left intraparietal activity driven by the naming of tools. Instead, this activity may relate to learned motor representations associated with the skillful use of familiar tools.

Introduction

The concept of affordances was first articulated by James Gibson (1979) who argued that an animal’s perception of its surroundings includes a description of how the environment and the objects within it influence the animal’s potential for action. Following these ideas, it was suggested that simply seeing an object automatically evokes movement representations consistent with the possible actions that could be performed on that particular object given its shape, size, orientation, and location. In other words, objects potentiate certain actions depending on their intrinsic and extrinsic visual properties and this translates into an increased level of neuronal activity within the representations underlying those actions. Some of the most compelling evidence in support of this proposal has come from neurophysiological studies in the macaque monkey. Several of these investigations have shown that grasping-related neurons in both the ventral premotor cortex (area F5) and the anterior intraparietal sulcus (area AIP) not only respond during the act of grasping but also during the passive viewing of graspable objects (Murata et al., 1997, Murata et al., 2000, Taira et al., 1990). Importantly, many of these visual responses were congruent with the motor properties encoded by the neurons. That is, those objects for which the cells responded most strongly during grasping actions were often the same objects that evoked the highest responses during viewing. These results indicate that neuronal populations dedicated to mediating specific object-directed actions can also be engaged during the simple viewing of objects in the absence of any overt movement.

More recently, some intriguing behavioral results from human psychophysical studies also suggest that simply viewing objects can activate motor representations consistent with the particular actions that the objects most strongly afford (Craighero et al., 2002, Derbyshire et al., 2006, Ellis and Tucker, 2000, Helbig et al., 2006, Symes et al., 2007, Tucker and Ellis, 1998, Tucker and Ellis, 2004, Vainio et al., 2006). For example, Tucker and Ellis (2004) showed that responses during an object categorization task are influenced by the graspable properties of the object. The authors had previously developed a response apparatus that simulated both a precision-type grasp (which requires the opposition of the thumb and index finger) and a power-type grasp (which requires the opposition of the fingers and the palm of the hand) (Ellis and Tucker, 2000). Using this apparatus they instructed subjects to decide if an object, presented in picture format, was man-made or natural. Responses that simulated a precision grasp were facilitated if the object under question afforded a precision grasp (e.g., a mushroom) and responses that simulated a power grasp were facilitated if the object under question afforded a power grasp (e.g., a cucumber). Moreover, these effects were also observed when the stimuli were not the images of the objects but rather simply their written names. This last finding suggests that simply thinking about the concept of an object is enough to automatically evoke motor representations associated with grasping it.

In parallel with this line of research, human neuroimaging studies have described a number of areas within the posterior parietal cortex (PPC) as specialized for the control of particular actions (for reviews, see Culham et al., 2006, Culham and Valyear, 2006). Analogous to the functional organization within the macaque monkey PPC (for review, see Colby and Goldberg, 1999), a discrete region at the anterior end of the intraparietal sulcus (IPS) has been implicated in the guidance and control of object-directed grasping (Binkofski et al., 1998, Culham et al., 2003, Frey et al., 2005). Activity within this region, referred to as human area AIP, was elevated during grasping actions relative to reaching actions (Culham et al., 2003) and the grasp-related activation was not merely due to somatosensory stimulation (Culham, 2004). Critical to the current discussion, this grasping-related area also appears to respond during object viewing in the absence of any movement (Grèzes et al., 2003a, Grèzes et al., 2003b, Grèzes and Decety, 2002). These findings have been interpreted as evidence in support of the idea that an object’s visual affordances can activate specific motor representations; in this case, an object’s graspable properties activate motor modules specialized for grasping.

Other imaging research has reliably shown selectivity for familiar tools within the PPC, particularly in the left hemisphere (for reviews, see Johnson-Frey, 2004, Lewis, 2006). Some of these activation foci appear close to area AIP and it has been suggested that this activity relates to the hand actions associated with using familiar tools (Chao and Martin, 2000). However, perhaps what becomes activated within the PPC is not so much those motor representations specialized for using tools but rather those more generally associated with object-directed grasping. In other words, perhaps this tool-related activity reflects processing within the visuomotor system specialized for grasping, driven by the perceived ‘graspability’ of tools. A recent imaging study by Creem-Regehr and Lee (2005) aimed to test this possibility. The authors compared the activations associated with novel graspable objects to those associated with familiar tools. Their results revealed that during passive viewing, tool stimuli exclusively activated motor-related parieto-frontal areas. These results were interpreted to reflect an interaction between the functional identity of the tool and its perceived potential for action. However, since the two stimulus categories also differed in their overall familiarity, including the strength and extent of the sensorimotor experiences associated with them, perhaps the pattern of activity that was observed simply reflected these differences. Moreover, the unfamiliar “graspable” shapes were presented as 2D images with no cues as to their real world size and thus their graspability. Therefore, as the authors noted, it was uncertain whether the subjects perceived the shapes as graspable or not.

The purpose of the present study was to further investigate whether the intraparietal activity associated with tool naming simply reflects the fact that tools afford grasping, whereas typical control stimuli do not (e.g., Chao and Martin, 2000, used images of animals as control stimuli and animals do not typically afford grasping). To evaluate this possibility we measured responses during the naming of familiar objects that varied with respect to their graspability. Within each individual, we identified the intraparietal area selective for naming images of tools (vs. animals, as in Chao and Martin, 2000) and then examined the activity within this area during the naming of familiar tools, familiar graspable objects, and familiar non-graspable objects. The aim here was to evaluate whether or not responses within this area would generalize to other objects that were graspable but did not have the functional properties of tools. We also examined the combined group data using a whole-volume voxel-wise approach. To identify areas showing selectivity for tools we contrasted naming tools vs. naming graspable objects, and to identify areas sensitive to object graspability we contrasted naming graspable vs. non-graspable objects. At the same time, in a subset of subjects, we compared parietal activations associated with real grasping actions to those associated with naming tools. If the tool-related activity within the intraparietal cortex was being driven by the graspable properties of tools, perhaps reflecting the automatic activation of motor programs associated with grasping, then we would predict the following: (i) responses within the region should also be elevated during the naming and viewing of other graspable objects compared with non-graspable objects; and (ii) the region should show significant spatial overlap with area AIP as defined by real grasping (vs. reaching) actions. Alternatively, if the activity within this region was to reflect processing specifically related to tools then we would expect the area to respond selectively to our tool stimuli and not to our other categories of objects and perhaps also to be distinct from AIP.

Preliminary data from this project have previously been presented in abstract form.

Section snippets

Subjects

Eleven neurologically intact individuals participated in the study (five female; age range of 22–35). All were right-handed, with normal or corrected-to-normal visual acuity and all were naive to the goals of the study. Each participant provided informed consent according to procedures approved by the University of Western Ontario Health Sciences Review Ethics Board.

Stimuli

Visual stimuli were presented using a PC laptop connected to a video projector. Images were shown on a rear-projection screen

ROI analysis

All three ROIs that had been identified using an independent localizer (naming tools vs. animals) – the left AIPC, the left LTOC, and the left IFC – demonstrated a preference for tools but not graspable objects in the experimental runs (see Fig. 2). Specifically, in each of these three areas, the activation during the naming of tools was higher than during the naming of graspable objects; however, activation levels during the naming of graspable and non-graspable objects were comparable.

Most

Discussion

The goal of this study was to evaluate if the intraparietal activity driven by tool naming could be accounted for simply by the graspable nature of tools (compared to control stimuli used in previous studies, such as animals) or whether it was due to additional factors such as the functionality of tools. Our results revealed an area within the left intraparietal cortex that was active for tools but not other graspable objects, and responses to graspable and non-graspable objects did not differ.

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