Impaired access to manipulation features in Apraxia: Evidence from eyetracking and semantic judgment tasks
Introduction
Many everyday objects involve distinctive manipulations with certain motor movements appropriate to their intended usage. A doorknob, for instance, is typically associated with grabbing and turning motions. These motion properties are not only involved in manipulating an object physically, but also are intrinsic to the representation of the object itself as we think and talk about it. Supporting this line of thinking, Myung, Blumstein, and Sedivy (2006) showed that the similarity of manipulation features among objects affects their lexical-semantic processing. In an auditory lexical decision task, participants made a significantly faster decision about the target word (e.g., ‘typewriter’) following a related prime that shared manipulation features with the target (e.g., ‘piano’) than an unrelated prime (e.g., ‘blanket’).2 In an eye tracking study, participants looked at the manipulation-related picture (e.g., “typewriter”) significantly more often than the unrelated ones (e.g., “bucket/chisel”) or the visual control (e.g., “couch”) when asked to touch the corresponding object on a display in response to an auditory input (e.g., ‘piano’). These results suggest that perceptuomotor-based experiences play a critical role in object representation and support the claims made by the perceptual symbol systems theory or the notion of cognitive embodiment (e.g., Barsalou, 1999, Barsalou et al., 2003, Garbarini and Adenzato, 2004).
The idea underlying the perceptual symbol systems theory or cognitive embodiment is not a recent development, but has a long history (see Barsalou (1999) for an overview). Lissauer (1890), for instance, postulated a multi-modal account of object recognition and semantic memory, in which semantic information includes the visual and functional properties of an object as well as the sound and the characteristic motor patterns associated with it. Allport (1985) also proposed a distributed semantic architecture in which objects are represented by visual, tactile and motor/proprioceptive nodes in proportion to the extent to which these various sensorimotor systems were involved as the concept was initially acquired and further elaborated.
Similarly, the perceptual symbol systems theory postulates that perceptual and conceptual processes share cognitive and neural resources and/or mechanisms, and that conception is grounded in perception. In this view, conceptual tasks recruit the same brain areas (or at least the areas approximate to them) as those used in related perceptual processes). Thus, according to the perceptual symbol systems theory, a deficit in perceptuomotor processes should be accompanied by a deficit in accessing conceptual representations that make use of these processes. If this were the case then, a deficit in physically manipulating objects should result in a concomitant impairment in the semantic representations of objects in which manipulation features are an intrinsic property. Apraxia provides a unique means of investigating this issue.
Apraxia is a neurological disorder of skilled movements without musculature weaknesses or motor impairments. A patient with ideomotor apraxia exhibits an inability to pantomime the use of objects and has impaired gesture recognition. For example, patients may show an inability to correctly pantomime ‘how to salute,’ or ‘how to use a hammer.’ Ideomotor apraxic patients make spatiotemporal errors in praxis with regard to amplitude, trajectory, and timing, even when imitating (Buxbaum, 2001, Koski et al., 2002). To examine the relationship between manipulation action (e.g., gesture) and manipulation knowledge, Buxbaum and Saffran (2002) tested a group of left hemisphere brain-damaged apraxic and non-apraxic subjects on tool and animal knowledge, body part knowledge, and manipulation and function knowledge. They hypothesized that given apraxic patients’ deficit in skilled movements, they should perform worse on tool knowledge, body part knowledge, and manipulation knowledge than non-apraxic patients. For each test, patients were given either a picture triplet or a word triplet or both and were asked to point to the two most similar items (e.g., “ruler,” “plug,” “tape measure” for tool knowledge; “raccoon,” “leopard,” “lion” for animal knowledge; ‘elbow,’ ‘knee,’ ‘neck’ for body part knowledge; egg beater, pencil sharpener, hedge clipper for manipulation knowledge; tape, stapler, pen for function knowledge). As predicted, apraxic patients performed worse on tool than animal knowledge (non-apraxics displayed the opposite pattern). Apraxics were also more impaired in body part knowledge than non-apraxics. Most importantly, apraxics were relatively impaired in manipulation knowledge, while non-apraxics tended to be relatively impaired in function knowledge. These patterns indicate an association between gestural praxis impairment and a deficit in the conceptual representation of skilled movements, consistent with the theoretical framework of the perceptual symbol systems. Furthermore, the lesions of the apraxic patients in the left frontoparietal areas either overlapped or were in close proximity to those involved in conceptually processing manipulable objects (e.g., Boronat et al., 2005, Chao and Martin, 2000, Kellenbach et al., 2003).
Buxbaum and Saffran’s study used explicit semantic judgment tasks, however, and it is often the case that brain-injured patients show differences in their performance on explicit versus implicit tasks. For instance, Wernicke’s patients, who are severely impaired in auditory comprehension and show poor performance on explicit semantic judgment tasks, exhibit semantic priming in a lexical decision task where the semantic relationship between the prime and target word pairs is implicit. Such findings suggest that these patients are able to access lexical semantic relations, although they may fail to explicitly act on them (e.g., Blumstein et al., 1982, Milberg and Blumstein, 1981). It is possible that apraxic patients who fail to show sensitivity to manipulation features in an explicit task may show intact manipulation knowledge using an implicit task; this would imply that implicit manipulation knowledge is preserved. Alternatively, a failure of these patients to show sensitivity to manipulation knowledge in an implicit task would provide strong support for the association between gestural praxis and manipulation knowledge, and more generally the association between perceptuomotor processes and their conceptual representations.
To this end, Experiment 1 examined whether apraxic patients would show a deficit in manipulation knowledge when performing an implicit task. In an earlier study, Myung and colleagues (2006) showed that the eye tracking paradigm provides a sensitive measure of manipulation knowledge representation without requiring an explicit response about the manipulation properties of the stimuli. Moreover, this paradigm has been used successfully with brain-injured patients to examine on-line lexical processing (Yee, Blumstein, & Sedivy, 2008). Experiment 2 tested the same patients as in Experiment 1 using an explicit semantic judgment task comparable to the explicit task used by Buxbaum and Saffran (2002). Thus, Experiments 1 and 2 aimed to explore implicit and explicit processing of manipulation knowledge in apraxic patients and to elucidate whether a specific deficit in producing and/or comprehending skilled movements is associated with a deficit in the lexical-semantic representation of manipulable objects—even in an implicit task. Experiment 1 was conducted prior to Experiment 2 to make certain that any effect found in the implicit task of Experiment 1 was not contaminated with conscious activation of manipulation features called for in the explicit semantic judgment task of Experiment 2.
Section snippets
Experiment 1
Experiment 1 sought to determine whether apraxic patients would show an effect of manipulation similarity in an implicit task using the eye tracking paradigm. In order to investigate this question, it is necessary to ensure that a failure to show sensitivity to manipulation knowledge is not secondary to a more generalized deficit in access to lexical-semantic information. Therefore, in addition to investigating sensitivity to manipulation knowledge, Experiment 1 also assessed access to
Experiment 2: semantic judgment task
In a recent study, Buxbaum and colleagues (e.g., Buxbaum and Saffran, 2002, Buxbaum et al., 2000) investigated apraxic patients’ sensitivity to manipulation features using an explicit task in which subjects were asked to choose the two items out of three that were most similar to each other in terms of their manipulation. Since such a task overtly requires patients to retrieve the manipulation features of the objects, the nature and demands of the task are very different from those of an
General discussion
Experiments 1 and 2 investigated the processing of manipulation features in apraxic patients and non-apraxic brain-damaged controls. The results of Experiment 1 suggested that both the apraxic patients and the non-apraxic patients were sensitive to manipulation similarity among objects, but that this sensitivity was somewhat delayed in the apraxic patients. The results of Experiment 2 showed that the apraxic patients were significantly worse at making a semantic judgment on manipulation
Acknowledgments
This research was supported in part by NIH Grants NIDCD00314 to Brown University, NIDCD0081 to the Boston University School of Medicine, NIH Grant MH62566 to Julie Sedivy, NIH Grant MH070850 to Sharon L. Thompson-Schill, and NIH Grants NS36387 and HD050836 to Laurel Buxbaum. This material is the result of work supported by resources and the use of facilities at the Department of Veterans Affairs Medical Centers in Boston, MA and Providence, RI. The views expressed in this article are those of
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Department of Psychology, University of Calgary, Calgary, AB, Canada.