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      Extending the Reach of Tooling Theory: A Neurocognitive and Phylogenetic Perspective

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          Abstract

          Tool use research has suffered from a lack of consistent theoretical frameworks. There is a plethora of tool use definitions and the most widespread ones are so inclusive that the behaviors that fall under them arguably do not have much in common. The situation is aggravated by the prevalence of anecdotes, which have played an undue role in the literature. In order to provide a more rigorous foundation for research and to advance our understanding of the interrelation between tool use and cognition, we suggest the adoption of Fragaszy and Mangalam’s (2018) tooling framework, which is characterized by the creation of a body-plus-object system that manages a mechanical interface between tool and surface. Tooling is limited to a narrower suite of behaviors than tool use, which might facilitate its neurocognitive investigation. Indeed, evidence in the literature indicates that tooling has distinct neurocognitive underpinnings not shared by other activities typically classified as tool use, at least in primates. In order to understand the extent of tooling incidences in previous research, we systematically surveyed the comprehensive tool use catalog by Shumaker et al. (2011). We identified 201 tool use submodes, of which only 81 could be classified as tooling, and the majority of the tool use examples across species were poorly supported by evidence. Furthermore, tooling appears to be phylogenetically less widespread than tool use, with the greatest variability found in the primate order. However, in order to confirm these findings and to understand the evolution and neurocognitive mechanisms of tooling, more systematic research will be required in the future, particularly with currently underrepresented taxa.

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          Most cited references115

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          Grasping objects: the cortical mechanisms of visuomotor transformation.

          Grasping requires coding of the object's intrinsic properties (size and shape), and the transformation of these properties into a pattern of distal (finger and wrist) movements. Computational models address this behavior through the interaction of perceptual and motor schemas. In monkeys, the transformation of an object's intrinsic properties into specific grips takes place in a circuit that is formed by the inferior parietal lobule and the inferior premotor area (area F5). Neurons in both these areas code size, shape and orientation of objects, and specific types of grip that are necessary to grasp them. Grasping movements are coded more globally in the inferior parietal lobule, whereas they are more segmented in area F5. In humans, neuropsychological studies of patients with lesions to the parietal lobule confirm that primitive shape characteristics of an object for grasping are analyzed in the parietal lobe, and also demonstrate that this 'pragmatic' analysis of objects is separated from the 'semantic' analysis performed in the temporal lobe.
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            Representation of manipulable man-made objects in the dorsal stream.

            We used fMRI to examine the neural response in frontal and parietal cortices associated with viewing and naming pictures of different categories of objects. Because tools are commonly associated with specific hand movements, we predicted that pictures of tools, but not other categories of objects, would elicit activity in regions of the brain that store information about motor-based properties. We found that viewing and naming pictures of tools selectively activated the left ventral premotor cortex (BA 6). Single-unit recording studies in monkeys have shown that neurons in the rostral part of the ventral premotor cortex (canonical F5 neurons) respond to the visual presentation of graspable objects, even in the absence of any subsequent motor activity. Thus, the left ventral premotor region that responded selectively to tools in the current study may be the human homolog of the monkey canonical F5 area. Viewing and naming tools also selectively activated the left posterior parietal cortex (BA 40). This response is similar to the firing of monkey anterior intraparietal neurons to the visual presentation of graspable objects. In humans and monkeys, there appears to be a close link between manipulable objects and information about the actions associated with their use. The selective activation of the left posterior parietal and left ventral premotor cortices by pictures of tools suggests that the ability to recognize and identify at least one category of objects (tools) may depend on activity in specific sites of the ventral and dorsal visual processing streams.
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              Neural correlates of category-specific knowledge.

              An intriguing and puzzling consequence of damage to the human brain is selective loss of knowledge about a specific category of objects. One patient may be unable to identify or name living things, whereas another may have selective difficulty identifying man-made objects. To investigate the neural correlates of this remarkable dissociation, we used positron emission tomography to map regions of the normal brain that are associated with naming animals and tools. We found that naming pictures of animals and tools was associated with bilateral activation of the ventral temporal lobes and Broca's area. In addition, naming animals selectively activated the left medial occipital lobe--a region involved in the earliest stages of visual processing. In contrast, naming tools selectively activated a left premotor area also activated by imagined hand movements, and an area in the left middle temporal gyrus also activated by the generation of action words. Thus the brain regions active during object identification are dependent, in part, on the intrinsic properties of the object presented.
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                Author and article information

                Journal
                101506764
                Top Cogn Sci
                Top Cogn Sci
                Topics in cognitive science
                1756-8757
                1756-8765
                01 October 2021
                24 June 2021
                08 July 2024
                23 July 2024
                : 13
                : 4
                : 548-572
                Affiliations
                Comparative Cognition Unit, Messerli Research Institute, University of Veterinary Medicine Vienna ( https://ror.org/01w6qp003) , University of Vienna ( https://ror.org/03prydq77) , Medical University of Vienna ( https://ror.org/05n3x4p02)
                Author notes
                Correspondence should be sent to Jennifer A. D. Colbourne, Comparative Cognition Unit, Messerli Research Institute, University of Veterinary Medicine Vienna, 1210 Vienna, Austria. jadcolbourne@ 123456gmail.com
                Article
                EMS196466
                10.1111/tops.12554
                7616289
                34165917
                1e967429-3f35-4ee5-966a-0722394c5c80

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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                Categories
                Article

                animal behavior,animal tool use,evolution of technology,comparative cognition,object manipulation,spatial relations,tooling,replication crisis

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