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Brain structures playing a crucial role in the representation of tools in humans and non-human primates

Published online by Cambridge University Press:  15 June 2012

Guido Gainotti
Affiliation:
Department of Neurosciences, Neuropsychology Center, Policlinico Gemelli, Catholic University of Rome, Largo A. Gemelli, 8Italy. gainotti@rm.unicatt.it

Abstract

The cortical representation of concepts varies according to the information critical for their development. Living categories, being mainly based upon visual information, are bilaterally represented in the rostral parts of the ventral stream of visual processing; whereas tools, being mainly based upon action data, are unilaterally represented in a left-sided fronto-parietal network. The unilateral representation of tools results from involvement in actions of the right side of the body.

Type
Open Peer Commentary
Copyright
Copyright © Cambridge University Press 2012

In his stimulating target article, Vaesen rightly suggests that the obvious superiority of humans, in comparison with non-human primates, in tool use may result from several (social and non-social) cognitive capacities that differentiate them from other animals. Now, as each of these cognitive capacities is subsumed by specific cortical networks, the problem that I would take into account in my commentary concerns the brain structures that could play a critical role in the conceptual representation of tools in humans versus non-human primates. My commentary will be based on empirical data (obtained in anatomo-clinical studies or neuroimaging experiments, mainly conducted in humans) interpreted according to the principles of the “embodied cognition theories” (Barsalou Reference Barsalou2008) and of the “sensory-motor model of semantic knowledge” (Gainotti Reference Gainotti2006).

According to these principles, concepts are not represented in the brain in a formal, abstract manner, totally unrelated to the brain processing of sensory-motor functions (e.g., Fodor Reference Fodor1987); instead, they are represented in the same format in which they have been constructed by the sensory-motor system. Furthermore, the brain organization of categorical knowledge reflects the importance of the sensory-motor mechanisms that have mainly contributed to the development of each category.

From the anatomical point of view, these principles predict a close relationship between cortical areas crucially involved in a given category and localization of the sensorimotor mechanisms that have mainly contributed to the development of that category. These predictions have been confirmed by results obtained studying the neuro-anatomical correlates of category-specific semantic disorders and the brain areas activated by different conceptual categories during functional brain imaging experiments (see for reviews Barsalou Reference Barsalou2008; Gainotti Reference Gainotti2006). Both anatomo-clinical and functional neuroimaging experiments have, indeed, shown that living categories, such as “animals” and “plant life,” are bilaterally represented in the rostral and ventral parts of the temporal lobes, because their knowledge is mainly based on the integration of highly processed visual data with other perceptual information. On the contrary, artefacts (and in particular, tools) are unilaterally represented in a left-sided fronto-parietal network, because these categories are mainly based upon action and somatosensory data. Obviously, it is almost impossible to match the brain correlates of the “tools” category in humans and in non-human primates, because, as rightly remarked by Vaesen in his target article, primates in the wild use for food retrieval whatever they come across. Their lack of permanent functional attributions (functional fixedness) implies the impossibility of constructing a category characterized by functional features, such as tools. The study of the brain representation of objects in non-human primates has, therefore almost uniquely concerned the ventral stream of visual processing, where important similarities have been found between humans and non-human primates (e.g., Kriegeskorte et al. Reference Kriegeskorte, Mur, Ruff, Kiani, Bodurka, Esteky, Tanaka and Bandettini2008).

The impossibility of matching the brain correlates of tools in humans and non-human primates does not imply that the analysis of the brain structures playing a crucial role in the representation of tools in humans may not be relevant to understand the brain mechanisms that have allowed the development of the “tools” category and its astonishing complexity in humans. In particular, the left lateralization of fronto-parietal lesions observed in patients with a category-specific disorder for artefacts and the activation of the same left fronto-parietal areas during studies dealing with tools can be explained by two lateralized factors (handedness and language functions) that have been extensively discussed by Vaesen in his target article.

Handedness has been considered as a factor contributing to the development of tools in humans because lateralization enhances manual precision and facilitates motor coordination in social learning tasks. On the other hand, language is deemed to have more contributed to the sophistication of human technologies than to the divergence between humans and other primates in the development of tools. This Vaesen position, which emphasizes more the contribution of handedness than that of language to the tool development is supported by two recent studies, conducted by Lewis et al. (Reference Lewis, Phinney, Brefczynski-Lewis and DeYoe2006) and by Willems et al. (Reference Willems, Toni, Hagoort and Casasanto2010) in strong right- and left-handers, to evaluate the role played by asymmetries in motor experience (right-handedness) and by the left dominance for language on the left lateralization of tool representation. In the first study Lewis et al. (Reference Lewis, Phinney, Brefczynski-Lewis and DeYoe2006) have compared the pattern of cortical activation evoked by hand-manipulated tool sounds and by animal vocalizations, showing that tool sounds preferentially evoke activity in high-level motor-related cortical regions of the hemisphere opposite to the dominant hand. In the second study, Willems et al. (Reference Willems, Toni, Hagoort and Casasanto2010) used functional magnetic resonance imaging to compare premotor activity associated with understanding action verbs (strictly related to tool use) and showed that right-handers preferentially activated the left premotor cortex, whereas left-handers preferentially activated right premotor areas. In both studies, therefore, and in agreement with the positions defended by Vaesen in his target article, the laterality of cortical regions activated by the high-level action and tool use was related to right-handedness and not to the left-hemisphere dominance for language.

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