The neural bases of complex tool use in humans

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Abstract

The behaviors involved in complex human tool use cut across boundaries traditionally drawn between social, cognitive, perceptual and motor processes. Longstanding neuropsychological evidence suggests a distinction between brain systems responsible for representing: (1) semantic knowledge about familiar tools and their uses, and (2) the acquired skills necessary for performing these actions. Contemporary findings in functional neuroimaging support and refine this distinction by revealing the distributed neural systems that support these processes and the conditions under which they interact. Together, these findings indicate that behaviors associated with complex tool use arise from functionally specialized networks involving temporal, parietal and frontal areas within the left cerebral hemisphere.

Section snippets

Early and enduring insights from case studies of brain injury

Until very recently, our understanding of the brain mechanisms involved in representing complex tools and their usage came exclusively from studies of brain-injured patients suffering from apraxia – a disorder of learned, voluntary actions, or skills. Over a century ago, several European neurologists recognized that brain injury could selectively disrupt various processes necessary for skillful behaviors, including tool use 4, 5. Their observations began a tradition of apraxia research in

Distinguishing between conceptual and production systems

From as early as Morlass in 1928, it has been noted that brain damage could selectively impair conceptual knowledge about tools versus the skills necessary for their dexterous usage (cited in [6]). A schematic summarizing what was known about locations of brain lesions associated with conceptual versus production difficulties during the early 20th century is shown in Figure 1.

When asked to pantomime, or in some cases explicitly demonstrate, how a familiar tool is used, patients with conceptual

Representing knowledge of tools and associated actions

The difficulties experienced by Conceptual Apraxics can be interpreted as stemming from a form of semantic memory deficit [10]. Rothi and colleagues have argued that knowledge about actions, including tool use, might be represented in a specialized ‘action semantic system’ [22]. In addition, it has been proposed that the semantic system for action be fractionated further into separate subsystems for knowledge about tools, their functions, or how the appropriate actions associated with their

Representing acquired tool-use skills

As early as 1905 (Liepmann, [17]), it was known that damage to the left PPC could affect the ability to produce skills associated with tools (Figure 1). In the intervening century there have been a variety of attempts to explain this fact [4]. One class of theories posit that Ideomotor Apraxia reflects damage to a more general faculty unique to the left hemisphere, such as the ability to construct symbolic representations (i.e. asymbolia) [48], or to form actions on the basis of objects'

Conclusions

Our understanding of the neural bases of human tool use owes much to the observations of those who have studied behavioral deficits following brain injuries over the past 100 or more years (see also [59], in this issue). Indeed, as observed by early investigators, separate regions in the human left hemisphere are involved in representing conceptual knowledge concerning tools and their associated actions versus the acquired skills involved in their usage (Figure 1). These insights have been

Acknowledgements

Scott H. Johnson-Frey was formerly known as Scott H. Johnson. Preparation of this manuscript was supported by grants from NIMH (#MH002022–02) and the James S. McDonnell Foundation. This manuscript benefited from the constructive criticisms of the anonymous reviewers, and Valerie Gerry.

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