Elsevier

Neuropsychologia

Volume 48, Issue 1, January 2010, Pages 243-247
Neuropsychologia

Chimpanzees’ context-dependent tool use provides evidence for separable representations of hand and tool even during active use within peripersonal space

https://doi.org/10.1016/j.neuropsychologia.2009.09.010Get rights and content

Abstract

Considerable attention has been devoted to behaviors in which tools are used to perform actions in extrapersonal space by extending the reach. Evidence suggests that these behaviors result in an expansion of the body schema and peripersonal space. However, humans often use tools to perform tasks within peripersonal space that cannot be accomplished with the hands. In some of these instances (e.g., cooking), a tool is used as a substitute for the hand in order to pursue actions that would otherwise be hazardous. These behaviors suggest that even during the active use of tools, we maintain non-isomorphic representations that distinguish between our hands and handheld tools. Understanding whether such representations are a human specialization is of potentially great relevance to understand the evolutionary history of technological behaviors including the controlled use of fire. We tested six captive adult chimpanzees to determine whether they would elect to use a tool, rather than their hands, when acting in potentially hazardous vs. nonhazardous circumstances located within reach. Their behavior suggests that, like humans, chimpanzees represent the distinction between the hand vs. tool even during active use. We discuss the implications of this evidence for our understanding of tool use and its evolution.

Introduction

The ability to accurately control movements of our limbs is believed to depend on the existence of a multimodal spatial representation of the body (i.e., body schema) that is continuously updated to reflect changes in posture. Evidence suggests that experience-dependent changes in the body schema may accompany the use of handheld tools (Berti and Frassinetti, 2000, Farne and Ladavas, 2000, Maravita et al., 2002, Witt et al., 2005). For instance, using sticks and rakes to extend our reach appears to induce an experience-dependent expansion of the body schema such that the representation of the actor's limb encompasses the space occupied by the entire tool, or merely its end-effector (Holmes, Calvert, & Spence, 2004). Neurophysiological data from macaque monkeys appears to be consistent with this limb remapping hypothesis (LRH). Although not natural tool users, through extended stimulus-response conditioning macaques can be trained to use a rake to retrieve out-of-reach food items. Remarkably, during rake use, the visual receptive fields of bimodal (visuo-tactile) parietal neurons, that initially code the location of the hand, appear to expand to cover the tool (Iriki, Tanaka, & Iwamura, 1996). As a result, space that was previously extrapersonal (beyond reach) is now represented as peripersonal (Maravita et al., 2001, Maravita and Iriki, 2004).

In the extreme, the LRH might be taken to suggest that formerly discrete representations of the hand or tool (or the space that they occupy) become isomorphic during tool use. However, the ability of actors to switch between use of the hand and tool fluently seems inconsistent with this possibility. Nevertheless, the issue of whether maintain a parallel representation of the natural (i.e., pre-tool use) body schema even during tool use, or are somehow capable of recalibrating the body schema instantaneously remains unresolved. The LRH provides a compelling account of the representations that may underlie the control of movements in which handheld tools are used to extend the reach of the upper limb into extrapersonal space. An argument can be made that, during most activities of daily living, tools and utensils are used to perform actions within our natural peripersonal space. Moreover, tools are frequently used in ways that we would never employ our hands. For instance, we will readily use a stick to stoke the hot embers of a campfire, or stir a pot of boiling soup with a wooden spoon. In these circumstances, the target of the actions may be located well within reach, but a tool is chosen as a substitute for the upper limb in order to avoid harm. These examples suggest that we maintain separate non-isomorphic representations of the hand vs. tool as concrete entities even when using handheld tools within our normal peripersonal space.

Although this common form of tool-mediated behavior has received little direct attention from body schema researchers (cf. Cardinali et al., 2009), one can speculate that representations that clearly demarcate the space occupied by the hand and the tool may have played a pivotal role in the evolution of technological behaviors. Such representations would be necessary to open niches too dangerous to exploit manually (e.g., animal burrows or submerged areas), due to the potential presence of hidden dangers, to foraging with tools (sticks). Perhaps more importantly, maintaining distinct representations of the hand and tool would seem necessary to realize the ability to interact safely with, and ultimately control, fire. The fossil record indicates that the controlled use of fire by hominds was present by the Plio-Pleistocene (James, 1989, Knecht, 1997, Schick and Toth, 1993), and resulted in vast expansions of diet and habitat.

Given the evolutionary significance of these tool-mediated behaviors, it is of considerable interest to determine whether or not similar evidence can be found in non-human species. It is well-established that our closest living relatives, chimpanzees (Pan troglodytes), manufacture and employ tools to probe for food in otherwise unreachable locations (Goodall, 1986, McGrew, 1992). However, it is currently unknown whether chimpanzees will elect to use a tool to obtain a reward that is within reach, but in a context that is perceived as potentially hazardous. If so, this would suggest that, even when using a tool, chimpanzees maintain internal representations that accurately differentiate the spatial properties of that object from their limbs. Further, such evidence would demonstrate that, like humans, chimpanzees’ use of tools is context-dependent, i.e., sensitive to their perception of personal risk. Such a demonstration would indicate that these context-dependent behaviors, predate modern humans.

To test this hypothesis, we investigated whether adult chimpanzees would elect to use their hands or a stick to remove a cover from a box that was well within reach, yet known to contain a food reward and/or an alarming object.

Section snippets

Participants and testing environment

Seven adult chimpanzees (age range 11.2–12.1 years) with extensive expertise using sticks and other tools to retrieve out-of-reach food rewards participated in this experiment. The study was approved by the IACUC at the University of Louisiana. The chimpanzees were living in a stable social group in a spacious indoor–outdoor compound at the University of Louisiana. Details of their living and testing environment and their experience using tools are described by Povinelli (2000). The animals

Results

All sessions were recorded on video from two perspectives (overhead and frontal). Two observers independently rated the trials using standardized written instructions. They recorded: (a) the number of trials on which the subjects used either the hand or tool to remove the cloth (condition A), and (b) the mean number of bouts in which the subjects used their hand or the tool to contact the box's contents (conditions A, B and C). One observer rated all trials and the second observer rated all

Discussion

The purpose of this study was to investigate whether chimpanzees, a species for whom the use of tools is natural, would elect to use a tool rather than their hand when performing a task located within peripersonal space, but perceived as potentially hazardous. If so, then this would be evidence that chimpanzees, like humans, maintain separate spatial representations of their hands and tools even when actively engaged in tool use. Results are consistent with this hypothesis. Our three main

Acknowledgments

We thank Jochen Barth, Anthony Rideaux, Laura Theall, Sarah Dunphy-Lelii, and Luke Brean for crucial assistance during the conduct and analysis of this study. The research reported in this article was approved by the University of Louisiana at Lafayette Institutional Animal Care and Use Committee and was conducted in accordance with all applicable laws of the Unites States of America. The work was funded by a James S. McDonnell Centennial Fellowship Award to DJP and James S. McDonnell Foundation

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