Elsevier

NeuroImage

Volume 21, Issue 4, April 2004, Pages 1224-1231
NeuroImage

Neural basis of pantomiming the use of visually presented objects

https://doi.org/10.1016/j.neuroimage.2003.11.017Get rights and content

Abstract

Neuropsychological studies of patients suffering from apraxia strongly imply a left hemisphere basis for skilful object use, the neural mechanisms of which, however, remain to be elucidated. We therefore carried out a PET study in 14 healthy human volunteers with the aim to isolate the neural mechanisms underlying the sensorimotor transformation of object-triggers into skilled actions. We employed a factorial design with two factors (RESPONSE: naming, pantomiming; and TRIGGER: actions, objects) and four conditions (IA: imitating the observed pantomime; IO: pantomiming the use of the object shown; NA: naming the observed pantomime; NO: naming the object shown). The design thus mainly aims at investigating the interaction [i.e. (IO–IA)–(NO–NA)] which allows the assessment of increased neural activity specific to the sensorimotor transformation of object-triggers into skilled actions. The results (P < 0.05, corrected) showed that producing a wide range of skilled actions triggered by objects (controlled for perceptual, motor, semantic, and lexical effects) activated left inferior parietal cortex. The data provide an explanation for why patients with lesions including left parietal cortex suffer from ideational apraxia as assessed by impaired object use and pontomining to visually presented objects (Brain 111 (1988) 1173; Cogn. Neuropsychol. 18 (2001) 671).

Introduction

One of the most basic of all human cognitive skills is the ability to use a very large range of objects by making sequences of object-specific actions: Although skilful object use has been observed in chimpanzees, apes are highly restricted in the variety of their habitual tool use (McGrew, 1993). Neuropsychological studies of patients suffering from apraxia suggest that this human capacity for highly skilful object use is a left hemisphere function De Renzi et al., 1968, Liepmann, 1905. A range of different conceptual frameworks has been used since to further characterize apraxia. One group of authors has adhered to Liepmann's original suggestion that one should distinguish between ideomotor and ideational apraxia. Patients with ideational apraxia suffer from a deficit of performing object-related skilled actions De Renzi and Lucchelli, 1988, De Renzi et al., 1968, Lehmkuhl and Poeck, 1981.

Acquiring skills in object use involves a variety of aspects. In many cases such as driving a car, it requires the development of a complex hierarchy of control structures, (which incidentally may also be present in apes, see Byrne, 2002). In others, such as those involved in many sports, exquisite timing in response to external triggers must be attained (see, e.g., McLeod, 1987). In yet others such as those needed in carpentry, it requires knowledge of naı̈ve physics (Goldenberg and Hagmann, 1998). One key ability common to all these skilful actions is, however, to acquire a set of routines each corresponding to specific learned components of a skill. In a more theoretical language, these routines could correspond to specific sets of parameter settings within a general system for the control of action, such as that suggested by Wolpert and Ghahramani (2000). A second key ability is to be able to elicit each of these components by a specific perceptual trigger (or triggers). When, for instance, a patient is presented with an object, and asked to use it (or to pantomime its use), he or she must have learned both the appropriate movement and its eliciting condition. For the second of these key abilities, it is well established that even low-level (visual) object characteristics may help to elicit an action appropriate to an object—Gibson's (1979) concept of affordance. In humans, the existence of such object-triggered affordances is supported by both experimental Rumiati and Humphreys, 1998, Tucker and Ellis, 1998 and neuropsychological Humphreys and Riddoch, 2002, Riddoch and Humphreys, 1998 evidence. Object-specific triggering cannot, however, just depend upon the low-level visual characteristics of objects; just consider the actions elicited by an electric plug, an electric iron, and so on.

The conceptual framework of Norman and Shallice (1980) extends the affordance concept by postulating the existence of an object trigger system which activates specific action schemata. A basic biased competition mechanism—called contention scheduling and implemented in Cooper and Shallice (2000)—then allows routine actions to be produced without conflict by activating relevant and inhibiting irrelevant schemata at appropriate times set by environmental triggers. Thus, a neuropsychological deficit observed in patients with left hemisphere lesions who show ideational apraxia (defined as a selective deficit in performing highly practiced actions involving objects; De Renzi and Lucchelli, 1988, Liepmann, 1905, Rumiati et al., 2001) can be interpreted as damage to or a disconnection between components of this system.

The complexity of the set of processes involved in the production of skilled actions is very difficult to analyze by standard lesion methods as complex skilful actions depend upon and modulate the already complex set of processes required in more basic visuomotor operations. In addition, neuropsychological attempts to analyze the neural basis of skilful object use have proved difficult because patients tend to have rather large lesions and additional deficits, for example, impaired imitation of actions, action or object agnosia, or aphasia. This neuropsychological dilemma (see Marshall and Fink, 2003) provides a special opportunity to use functional imaging to elucidate the organization of these subsystems which when damaged give rise to the relevant neuropsychological disorders. So far, however, functional imaging of object use has been limited to a highly restricted set of very simple actions such as grasping (Grafton et al., 1996a), also using various forms of grip (Grèzes et al., 2003), the manipulation of meaningless objects Binkofski et al., 1999, Grefkes et al., 2002, learning of one specific set of movements Jenkins et al., 1994, Stephan et al., 1995, or has used the analogy of “mental simulation” of the actions Decety et al., 1994, Grafton et al., 1996b, Stephan et al., 1995.

In this paper, we primarily aim at investigating whether there is evidence for specific mechanisms underlying the triggering of actions by objects. This is strongly suggested by neuropsychological evidence of utilization behavior following medial prefrontal lesions Lhermitte, 1983, Shallice et al., 1989. However, the locus of lesions which give rise to such effects—medial prefrontal cortex (see De Renzi and Barbieri, 1992)—corresponds to the impairment of parts of a Supervisory System which inhibits any such behavior rather than of the trigger system itself. It is therefore not relevant for localizing the trigger system. Based on animal neurophysiological data Rizzolatti et al., 1997, Sakata et al., 1995, Taira et al., 1990, functional imaging studies Binkofski et al., 1999, Grafton et al., 1996a, Grefkes et al., 2002 and, to some extent, neuropsychological studies of patients suffering from ideational apraxia De Renzi and Lucchelli, 1988, Rumiati et al., 2001, a more plausible hypothesis for the locus of the trigger system for action schemata, could be left inferior parietal cortex.

A major technical problem when employing functional magnetic resonance imaging to study the neural mechanisms underlying skilled actions is the production of movement artifacts as a result of performing the task. This has led some investigators to use tasks in which subjects are required to imagine performing the action Decety et al., 1994, Grafton et al., 1996b. In contrast, PET is less sensitive to movement artifacts and thus allows the assessment of proper skilful actions in the scanner. We accordingly performed a study in which normal volunteers produced 90 different skilful object-related pantomimes while lying in a PET scanner. We used pantomiming of object and tool use (rather than actual object and tool use) as this task predicts well and correlates with performance on actual object and tool use in apraxia De Renzi and Lucchelli, 1988, Goldenberg and Hagmann, 1998, but avoids practical problems such as object placement in the subjects' hands which causes difficulties in the scanning environment (e.g. timing, the necessity to have another person in the scanning room, etc.). In addition, it has been established in neuroimaging studies that the mere viewing of objects affords actions that can be performed with them (Grèzes and Decety, 2002). To isolate the neural mechanisms specific to object-triggered action schemata and their selection, we employed a factorial design with two factors (RESPONSE: naming, pantomiming; and TRIGGER: pantomimes, objects) and four conditions (IA: imitating the observed pantomime; IO: pantomiming the use of the object shown; NA: naming the observed pantomime; NO: naming the object shown). This contrast between object-triggering of an action and imitation is somewhat analogous to the procedure used for different forms of grip by Grèzes et al. (2003). The design controls for the perceptual, semantic, lexical, and sensorimotor aspects of both object- and action-related processing. The experimental design specifically focuses at investigating the interaction [i.e. (IO–IA)–(NO–NA)] which allows the assessment of increased neural activity specific to the selection of action schemata triggered by objects.

Section snippets

Subjects

Fourteen healthy right-handed males volunteers (mean age 26.14 ± 6.05 years) with no history of neurological or psychiatric illness gave informed consent. Handedness was assessed by the Edinburgh Inventory test (Oldfield, 1971). The study was approved by the ethics committee of the University Hospital of the RWTH—Aachen, Germany.

Experimental design and stimuli

A factorial design with the factors TRIGGER (objects and actions) and RESPONSE (pantomiming and naming) was employed. This results in four conditions: (i) IA, imitating

PET

Table 1, Table 2, Table 3, Table 4 show the local maxima of the areas of increased neural activity, as assessed by PET rCBF measurements, associated with the main effects. Analysis of the factor RESPONSE revealed the expected differential neural activations associated with pantomiming (relative to naming, Table 1) and with naming (relative to pantomiming, Table 2), respectively. Analysis of the factor TRIGGER revealed differential neural activations associated with object processing (relative

Discussion

The main purpose of this study was to establish the neural basis of pantomiming object and tool use in the normal human brain. We employed a pantomiming task as it predicts well actual object and tool use De Renzi and Lucchelli, 1988, Goldenberg and Hagmann, 1998 but it is easier to implement in a PET scanning environment. Our data extend previous imaging and neuropsychological data by allowing a specification of the areas sustaining the production of object-related pantomimes. The analysis of

Acknowledgements

The authors thank the PET group of the Research Center Jülich for assistance, and Ann Assmus, Nuh Rahbari, and Alessia Tessari for scoring the behavioral data. We thank C. Grefkes for providing the probability map of Brodmann area 6. This study was supported by the Deutsche Forschungsgemeinshaft (DFG-KFO 112) and the Alexander von-Humboldt Stiftung.

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