Decoding the neural mechanisms of human tool use.

Tool use is essential and culturally universal to human life, common to huntergatherer and modern advanced societies alike. Although the neuroscience of simpler visuomotor behaviours like reaching and grasping have been studied extensively, relatively little is known about the brain mechanisms underlying learned tool use.

Journal of …, 2012

MV. Closely overlapping responses to tools and hands in left lateral occipitotemporal cortex. perception of object-directed actions performed by either hands or tools recruits regions in left fronto-parietal cortex. Here, using functional MRI (fMRI), we tested whether the common role of hands and tools in object manipulation is also reflected in the distribution of response patterns to these categories in visual cortex. In two experiments we found that static pictures of hands and tools activated closely overlapping regions in left lateral occipitotemporal cortex (LOTC). Left LOTC responses to tools selectively overlapped with responses to hands but not with responses to whole bodies, nonhand body parts, other objects, or visual motion. Multivoxel pattern analysis in left LOTC indicated a high degree of similarity between response patterns to hands and tools but not between hands or tools and other body parts. Finally, functional connectivity analysis showed that the left LOTC hand/tool region was selectively connected, relative to neighboring body-, motion-, and object-responsive regions, with regions in left intraparietal sulcus and left premotor cortex that have previously been implicated in hand/tool action-related processing. Taken together, these results suggest that action-related object properties shared by hands and tools are reflected in the organization of high-order visual cortex. We propose that the functional organization of high-order visual cortex partly reflects the organization of downstream functional networks, such as the fronto-parietal action network, due to differences within visual cortex in the connectivity to these networks. action perception; functional connectivity; visual cortex; ventral stream Address for reprint requests and other correspondence: M. V. Peelen, Center for Mind/Brain Sciences

MV. Closely overlapping responses to tools and hands in left lateral occipitotemporal cortex. perception of object-directed actions performed by either hands or tools recruits regions in left fronto-parietal cortex. Here, using functional MRI (fMRI), we tested whether the common role of hands and tools in object manipulation is also reflected in the distribution of response patterns to these categories in visual cortex. In two experiments we found that static pictures of hands and tools activated closely overlapping regions in left lateral occipitotemporal cortex (LOTC). Left LOTC responses to tools selectively overlapped with responses to hands but not with responses to whole bodies, nonhand body parts, other objects, or visual motion. Multivoxel pattern analysis in left LOTC indicated a high degree of similarity between response patterns to hands and tools but not between hands or tools and other body parts. Finally, functional connectivity analysis showed that the left LOTC hand/tool region was selectively connected, relative to neighboring body-, motion-, and object-responsive regions, with regions in left intraparietal sulcus and left premotor cortex that have previously been implicated in hand/tool action-related processing. Taken together, these results suggest that action-related object properties shared by hands and tools are reflected in the organization of high-order visual cortex. We propose that the functional organization of high-order visual cortex partly reflects the organization of downstream functional networks, such as the fronto-parietal action network, due to differences within visual cortex in the connectivity to these networks. action perception; functional connectivity; visual cortex; ventral stream Address for reprint requests and other correspondence: M. V. Peelen, Center for Mind/Brain Sciences

Frontiers in human neuroscience, 2014

Functional neuroimaging studies have implicated the left lateral occipitotemporal cortex (LOTC) in both tool and hand perception but the functional role of this region is not fully known. Here, by using a task manipulation, we tested whether tool-/hand-selective LOTC contributes to the discrimination of tool-associated hand actions. Participants viewed briefly presented pictures of kitchen and garage tools while they performed one of two tasks: in the action task, they judged whether the tool is associated with a hand rotation action (e.g., screwdriver) or a hand squeeze action (e.g., garlic press), while in the location task they judged whether the tool is typically found in the kitchen (e.g., garlic press) or in the garage (e.g., screwdriver). Both tasks were performed on the same stimulus set and were matched for difficulty. Contrasting fMRI responses between these tasks showed stronger activity during the action task than the location task in both tool- and hand-selective LOTC r...

2012

Prior research has linked visual perception of tools with plausible motor strategies. Thus, observing a tool activates the putative action-stream, including the left posterior parietal cortex. Observing a hand functionally grasping a tool involves the inferior frontal cortex. However, tool-use movements are performed in a contextual and grasp specific manner, rather than relative isolation.

Cortex; a journal devoted to the study of the nervous system and behavior, 2013

Journal homepage: www.elsevier.com/locate/cortex c o r t e x 4 9 ( 2 0 1 3 ) 2 0 9 7 e2 1 0 5 0010-9452/$ e see front matter ª

2005

Determining the relationship betweenmechanisms involved in action planning and/or execution is critical to understanding the neural bases of skilled behaviors, including tool use. Herewe report findings from two fMRI studies of healthy, right-handed adults in which an event-related design was used to distinguish regions involved in planning (i.e. identifying, retrieving and preparing actions associated with a familiar tools ’ uses) versus executing tool use gestures with the dominant right (experiment 1) and non-dominant left (experi-ment 2) hands. For either limb, planning tool use actions activates a distributed network in the left cerebral hemisphere consisting of: (i) posterior superior temporal sulcus, along with proximal regions of the middle and superior temporal gyri; (ii) inferior frontal and ventral premotor cortices; (iii) two distinct parietal areas, one located in the anterior supramarginal gyrus (SMG) and another in posterior SMG and angular gyrus; and (iv) dorsolatera...

Journal of The International Neuropsychological Society, 2017

Objectives: Neuropsychological and neuroimaging evidence indicates that tool use knowledge and abilities are represented in the praxis representation network (PRN) of the left cerebral hemisphere. We investigated whether PRN would also underlie the planning of function-appropriate grasps of tools, even though such an assumption is inconsistent with some neuropsychological evidence for independent representations of tool grasping and skilled tool use. Methods: Twenty right-handed participants were tested in an event-related functional magnetic resonance imaging (fMRI) study wherein they planned functionally appropriate grasps of tools versus grasps of non-tools matched for size and/or complexity, and later executed the pantomimed grasps of these objects. The dominant right, and non-dominant left hands were used in two different sessions counterbalanced across participants. The tool and non-tool stimuli were presented at three different orientations, some requiring uncomfortable hand rotations for effective grips, with the difficulty matched for both hands. Results: Planning functional grasps of tools (vs. non-tools) was associated with significant asymmetrical increases of activity in the temporo/occipital-parieto-frontal networks. The greater involvement of the left hemisphere PRN was particularly evident when hand movement kinematics (including wrist rotations) for grasping tools and non-tools were matched. The networks engaged in the task for the dominant and non-dominant hand were virtually identical. The differences in neural activity for the two object categories disappeared during grasp execution. Conclusions: The greater hand-independent engagement of the left-hemisphere praxis representation network for planning functional grasps reveals a genuine effect of an early affordance/function-based visual processing of tools. (JINS, 2017, 23, 108-120

Brain, 2009

Misuse of tools and objects by patients with left brain damage is generally recognized as a manifestation of apraxia, caused by parietal lobe damage. The use of tools and objects can, however, be subdivided in several components. The purpose of our study was to find out which of these are dependent on parietal lobe function. Thirty-eight patients with left brain damage and aphasia were examined using tests to assess the retrieval of functional knowledge from semantic memory (Functional Associations), mechanical problem solving (Novel Tools) and use of everyday tools and objects (Common Tools). Voxel-wise analysis of magnetic resonance images revealed two regions where lesions had a significant impact on the test results. One extended rostrally from the central region and ventrally through the middle frontal cortex to the dorsal margin of the inferior frontal gyrus. The other reached dorsally and caudally from the supramarginal gyrus, through the inferior, to superior parietal lobe. Whereas the frontal lesions had an adverse influence on all experimental tests as well as on the subtests of the Aachen Aphasia test, parietal lesions impaired Novel and Common Tools, but did not have an adverse effect on the Functional Associates. An association between Functional Associations and temporal lesions became apparent when patients with only a selective deficit in the test were considered, but did not show up in the whole group analysis. The parietal influence was as strong for the selection as for the use of either novel or common tools, although choice of appropriate manual configuration and movements was more important for use than for selection. We conclude that the contribution of the parietal lobe to tool use concerns general principles of tool use rather than knowledge about the prototypical use of common tools and objects, and the comprehension of mechanical interactions of the tool with other tools, recipients or material rather than the selection of grip formation and manual movements.

Cerebral Cortex, 2004

Determining the relationship between mechanisms involved in action planning and/or execution is critical to understanding the neural bases of skilled behaviors, including tool use. Here we report findings from two fMRI studies of healthy, right-handed adults in which an event-related design was used to distinguish regions involved in planning (i.e. identifying, retrieving and preparing actions associated with a familiar tools' uses) versus executing tool use gestures with the dominant right (experiment 1) and non-dominant left (experiment 2) hands. For either limb, planning tool use actions activates a distributed network in the left cerebral hemisphere consisting of: (i) posterior superior temporal sulcus, along with proximal regions of the middle and superior temporal gyri; (ii) inferior frontal and ventral premotor cortices; (iii) two distinct parietal areas, one located in the anterior supramarginal gyrus (SMG) and another in posterior SMG and angular gyrus; and (iv) dorsolateral prefrontal cortex (DLFPC). With the exception of left DLFPC, adjacent and partially overlapping sub-regions of left parietal, frontal and temporal cortex are also engaged during action execution. We suggest that this left lateralized network constitutes a neural substrate for the interaction of semantic and motoric representations upon which meaningful skills depend.