Tool-body assimilation in the brain

eLife, 2013

Sophisticated tool use is a defining characteristic of the primate species but how is it supported by the brain, particularly the human brain? Here we show, using functional MRI and pattern classification methods, that tool use is subserved by multiple distributed action-centred neural representations that are both shared with and distinct from those of the hand. In areas of frontoparietal cortex we found a common representation for planned hand-and tool-related actions. In contrast, in parietal and occipitotemporal regions implicated in hand actions and body perception we found that coding remained selectively linked to upcoming actions of the hand whereas in parietal and occipitotemporal regions implicated in tool-related processing the coding remained selectively linked to upcoming actions of the tool. The highly specialized and hierarchical nature of this coding suggests that hand-and tool-related actions are represented separately at earlier levels of sensorimotor processing before becoming integrated in frontoparietal cortex.

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

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.

Cognitive Processing

Years ago, it was demonstrated (e.g., Rizzolatti et al. in Handbook of neuropsychology, Elsevier Science, Amsterdam, 2000) that the brain does not encode the space around us in a homogeneous way, but through neural circuits that map the space relative to the distance that objects of interest have from the body. In monkeys, relatively discrete neural systems, characterized by neurons with specific neurophysiological responses, seem to be dedicated either to represent the space that can be reached by the hand (near/peripersonal space) or to the distant space (far/extrapersonal space). It was also shown that the encoding of spaces has dynamic aspects because they can be remapped by the use of tools that trigger different actions (e.g., Iriki et al. 1998). In this latter case, the effect of the tool depends on the modulation of personal space, that is the space of our body. In this paper, I will review and discuss selected research, which demonstrated that also in humans: 1 spaces are e...

Cortex, 2007

In human and non human primates, evidence has been reported supporting the idea that near peripersonal space is represented through integrated multisensory processing. In humans, the interaction between near peripersonal space representation and action execution can be revealed in brain damaged patients through the use of tools that, by extending the reachable space, modify the strength of visual-tactile extinction, thus showing that tool-mediated actions modify the multisensory coding of near peripersonal space. For example, following the use of a rake to retrieve distant, otherwise non reachable objects, the peri-hand multisensory area has been documented to extend to include the distal part of a rake . The re-sizing of peri-hand space seems to be selective for tool-use, as directional motor activity alone (i.e., pointing without the tool) and visual/proprioceptive experience alone (protracted passive exposure to the tool) does not vary the extent of the visual-tactile peri-hand space . Moreover, the amount of dynamic resizing varies with the length of the used tool, and is specifically centred on the functionally relevant part of the tool . Here, besides reviewing and discussing these results, we report new evidence, based on a single-case study, supporting the idea that dynamic re-sizing of peri-hand space consists of a real spatial extension of the visual-tactile integrative area along the tool axis.

Human dexterity with tools is believed to stem from our ability to incorporate and use tools as parts of our body. However tool incorporation, evident as extensions in our body representation and peri-personal space, has been observed predominantly after extended tool exposures and does not explain our immediate motor behaviours when we change tools. Here we utilize two novel experiments to elucidate the presence of additional immediate tool incorporation effects that determine motor planning with tools. Interestingly, tools were observed to immediately induce a trial-by-trial, tool length dependent shortening of the perceived limb lengths, opposite to observations of elongations after extended tool use. Our results thus exhibit that tools induce a dual effect on our body representation; an immediate shortening that critically affects motor planning with a new tool, and the slow elongation, probably a consequence of skill related changes in sensory-motor mappings with the repeated use of the tool.

2014

The term affordance defines a property of objects, which relates to the possible interactions that an agent can carry out on that object. In monkeys, canonical neurons encode both the visual and the motor properties of objects with high specificity. However, it is not clear if in humans exists a similarly finegrained description of these visuomotor transformations. In particular, it has not yet been proven that the processing of visual features related to specific affordances induces both specific and early visuomotor transformations, given that complete specificity has been reported to emerge quite late (300-450 ms). In this study, we applied an adaptation-stimulation paradigm to investigate early corticospinal facilitation and hand movements' synergies evoked by the observation of tools. We adapted, through passive observation of finger movements, neuronal populations coding either for precision or power grip actions. We then presented the picture of one tool affording one of the two grasps types and applied single-pulse Transcranial Magnetic Stimulation (TMS) to the hand primary motor cortex, 150 ms after image onset. Cortico-spinal excitability of the Abductor Digiti Minimi and Abductor Pollicis Brevis showed a detailed pattern of modulations, matching tools' affordances. Similarly, TMS-induced hand movements showed a pattern of grip-specific whole hand synergies. These results offer a direct proof of the emergence of an early visuomotor transformation when tools are observed, that maintains the same amount of synergistic motor details as the actions we can perform on them.

Journal of Neurophysiology, 2011

The 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-...

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.

Neuroscience Letters, 2004

The effects of tool-use on the brain's representation of the body and of the space surrounding the body (‘peripersonal space’) has recently been studied within a number of disciplines in cognitive neuroscience, and is also of great interest to philosophers and behavioural ecologists. To date, most experimental findings suggest that tool-use extends the boundary of peripersonal space—visual stimuli presented at the tips of tools interact more with simultaneous tactile stimuli presented at the hands than visual stimuli presented at the same distance, but not associated with the tools. We studied the proposed extension of peripersonal space by tool-use by measuring the effects of three different tool-use tasks on the integration of visual and tactile stimuli at three distances from participants’ hands along two hand-held tools. When the tool-use task required using the shafts or the tips of the tools, visuotactile interactions were stronger at the tips of the tools than in the middle of the shaft. When the handles of the tools were used, however, visuotactile interactions were strongest near the hands and decreased with distance along the tools. These results suggest that tools do not simply ‘extend’ peripersonal space, but that just the tips of tools actively manipulated in extrapersonal space are incorporated into the brain's visuotactile representations of the body and of peripersonal space.