The Neuroscience of Human Tool Use

Valyear, Kenneth F.; Fitzpatrick, Aoife; McManus, E.F.

doi:10.1016/b978-0-12-804042-3.00112-3

Cited by 8 publications

(8 citation statements)

References 155 publications

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“…Our understanding of how the human brain represents object properties ( Kanwisher, 2010 ) and simple hand movements ( Gallivan and Culham, 2015 ) has significantly advanced in the last few decades; however, far less is known about the neural representations that underpin real actions involving 3D tools ( Valyear et al, 2017 ). Most neuroimaging experiments that investigate how tools and their associated actions are represented in the brain have used visual paradigms where objects and body parts are displayed as 2D images ( Ishibashi et al, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Hand-Selective Visual Regions Represent How to Grasp 3D Tools: Brain Decoding during Real Actions

et al. 2021

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Most neuroimaging experiments that investigate how tools and their actions are represented in the brain use visual paradigms where tools or hands are displayed as 2D images and no real movements are performed. These studies discovered selective visual responses in occipitotemporal and parietal cortices for viewing pictures of hands or tools, which are assumed to reflect action processing, but this has rarely been directly investigated. Here, we examined the responses of independently visually defined category-selective brain areas when participants grasped 3D tools (N=20; 9 females). Using real action fMRI and multi-voxel pattern analysis, we found that grasp typicality representations (i.e., whether a tool is grasped appropriately for use) were decodable from hand-selective areas in occipito-temporal and parietal cortices, but not from tool-, object-, or body-selective areas, even if partially overlapping. Importantly, these effects were exclusive for actions with tools, but not for biomechanically matched actions with control non-tools. In addition, grasp typicality decoding was significantly higher in hand than toolselective parietal regions. Notably, grasp typicality representations were automatically evoked even when there was no requirement for tool use and participants were naïve to object category (tool vs non-tools). Finding a specificity for typical tool grasping in hand-, rather than tool-, selective regions challenges the long-standing assumption that activation for viewing tool images reflects sensorimotor processing linked to tool manipulation. Instead, our results show that typicality representations for tool grasping are automatically evoked in visual regions specialised for representing the human hand, the brain's primary tool for interacting with the world. Significance StatementThe unique ability of humans to manufacture and use tools is unsurpassed across the animal kingdom, with tool use considered a defining feature of our species. Most neuroscientific studies that investigate the brain mechanisms that support tool use, record brain activity while people simply view images of tools or hands and not when people perform actual hand movements with tools. Here we show that specific areas of the human visual system that preferentially process hands automatically encode how to appropriately grasp 3D tools, even when no actual tool use is required. These findings suggest that visual areas optimized for processing hands represent 3 fundamental aspects of tool grasping in humans, such as which side they should be grasped for 66 correct manipulation.

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Section: Discussionmentioning

confidence: 99%

Hand-Selective Visual Regions Represent How to Grasp 3D Tools: Brain Decoding during Real Actions

et al. 2021

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“…We adopted the tool localizer to identify the ROIs independently from the main experiment (see the previous section). The selected ROIs within the tool network included: the left dorsal premotor cortex (PMd), at the junction between the precentral sulcus and the superior frontal sulcus (Valyear et al 2012 ; Gallivan et al 2013c ), the left ventral premotor cortex (PMv), located within the precentral gyrus (Gallivan et al 2011 , 2013c ; Valyear et al 2012 ), the left superior parietal lobule (SPL), located posteriorly to the postcentral sulcus and superiorly to the intraparietal sulcus (Lewis 2006 ), the left superior-parieto-occipital cortex (SPOC) in the superior end of the parieto-occipital sulcus (Vesia et al 2010 ; Gallivan et al 2013c ), the left anterior intraparietal sulcus (aIPS) located in the junction between intraparietal sulcus and postcentral sulcus (Culham et al 2003 ; Grefkes and Fink 2005 ; Valyear et al 2007 ; Valyear and Culham 2010 ; Gallivan et al 2013c ), the left supramarginal gyrus (SMG), lateral to the segment of IPS and posterior to the lateral sulcus (Lewis 2006 ; Gallivan et al 2013c ), the left posterior middle temporal gyrus (pMTG) within the posterior portion of the ventral stream (Gallivan et al 2013c ), the left primary motor area (M1), identified in the ‘hand knob’ along the anterior part of the central sulcus (Yousry 1997 ), has been localized adopting a univariate contrast from the main experiment (execution vs baseline, see below). …”

Section: Methodsmentioning

confidence: 99%

“…the left dorsal premotor cortex (PMd), at the junction between the precentral sulcus and the superior frontal sulcus (Valyear et al 2012 ; Gallivan et al 2013c ),…”

Section: Methodsmentioning

confidence: 99%

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Neural encoding and functional interactions underlying pantomimed movements

Malfatti

Turella

2021

Brain Struct Funct

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Pantomimes are a unique movement category which can convey complex information about our intentions in the absence of any interaction with real objects. Indeed, we can pretend to use the same tool to perform different actions or to achieve the same goal adopting different tools. Nevertheless, how our brain implements pantomimed movements is still poorly understood. In our study, we explored the neural encoding and functional interactions underlying pantomimes adopting multivariate pattern analysis (MVPA) and connectivity analysis of fMRI data. Participants performed pantomimed movements, either grasp-to-move or grasp-to-use, as if they were interacting with two different tools (scissors or axe). These tools share the possibility to achieve the same goal. We adopted MVPA to investigate two levels of representation during the planning and execution of pantomimes: (1) distinguishing different actions performed with the same tool, (2) representing the same final goal irrespective of the adopted tool. We described widespread encoding of action information within regions of the so-called “tool” network. Several nodes of the network—comprising regions within the ventral and the dorsal stream—also represented goal information. The spatial distribution of goal information changed from planning—comprising posterior regions (i.e. parietal and temporal)—to execution—including also anterior regions (i.e. premotor cortex). Moreover, connectivity analysis provided evidence for task-specific bidirectional coupling between the ventral stream and parieto-frontal motor networks. Overall, we showed that pantomimes were characterized by specific patterns of action and goal encoding and by task-dependent cortical interactions.

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“…2), which may mediate stable object "affordances" (i.e., action representations closely associated with a given object) as part of skilled object perception (Binkofski & Buccino, 2006;Binkofski, Buccino, Zilles, & Fink, 2004;Sakreida et al, 2016). In fact, the observed connectivity pattern represents major parts of the so-called "tool network" (Lewis, 2006;Valyear, Fitzpatrick, & McManus, 2017). This network is recruited during the perception of tools and the execution of tool-related actions.…”

Section: Skilled Object Recognitionmentioning

confidence: 99%

A network view on brain regions involved in experts’ object and pattern recognition: Implications for the neural mechanisms of skilled visual perception

Langner

Eickhoff

Bilalić

2019

Brain and Cognition

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Skilled visual object and pattern recognition form the basis of many everyday behaviours. The game of chess has often been used as a model case for studying how long-term experience aides in perceiving objects and their spatio-functional interrelations. Earlier research revealed two brain regions, posterior middle temporal gyrus (pMTG) and collateral sulcus (CoS), to be linked to chess experts' superior object and pattern recognition, respectively. Here we elucidated the brain networks these two expertise-related regions are embedded in, employing resting-state functional connectivity analysis and meta-analytic connectivity modeling with the BrainMap database. pMTG was preferentially connected with dorsal visual stream areas and a parieto-prefrontal network for action planning, while CoS was preferentially connected with posterior medial cortex and hippocampus, linked to scene perception, perspective-taking and navigation. Functional profiling using BrainMap meta-data revealed that pMTG was linked to semantic processing as well as inhibition and attention, while CoS was linked to face and shape perception as well as passive viewing. Our findings suggest that pMTG subserves skilled object recognition by mediating the link between object identity and object affordances, while CoS subserves skilled pattern recognition by linking the position of individual objects with typical spatio-functional layouts of their environment stored in memory.

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The Neuroscience of Human Tool Use

Cited by 8 publications

References 155 publications

Hand-Selective Visual Regions Represent How to Grasp 3D Tools: Brain Decoding during Real Actions

Hand-Selective Visual Regions Represent How to Grasp 3D Tools: Brain Decoding during Real Actions

Neural encoding and functional interactions underlying pantomimed movements

A network view on brain regions involved in experts’ object and pattern recognition: Implications for the neural mechanisms of skilled visual perception

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