Claudio Brozzoli

Tool-use induces morphological updating of the body schema

Summary To control bodily movements the human brain relies on a somatosensory representation referred to as the body schema [1]. The almost century-old hypothesis that tool-use induces plastic changes resulting in the tool being incorporated in the body schema is nowadays widely accepted. Whether this somatosensory representation is truly modified remains unknown, however, as tool-use has never been shown to affect arm motor behaviour. Here we report that using a mechanical grabber that physically extends the arm does alter the kinematics of subsequent free-hand grasping movements. Remarkably, tool-use after-effects generalise to pointing movements, despite the absence of specific tool-training. Furthermore, this effect is driven by an increase of the represented length of the arm: after tool-use, subjects localised touches delivered on the elbow and middle fingertip of their arm as if they were farther apart. These findings indicate that tool-use alters the body schema, and also show that what is modified is the somatosensory representation of intrinsic properties of the body morphology.

That's Near My Hand! Parietal and Premotor Coding of Hand-Centered Space Contributes to Localization and Self-Attribution of the Hand

The ability to identify and localize our own limbs is crucial for survival. Indeed, the majority of our interactions with objects occur within the space surrounding the hands. In non-human primates, neurons in the posterior parietal and premotor cortices dynamically represent the space near the upper limbs in hand-centered coordinates. Neuronal populations selective for the space near the hand also exist in humans. It is unclear whether these remap the peri-hand representation as the arm is moved in space. Furthermore, no combined neuronal and behavioral data are available about the possible involvement of peri-hand neurons in the perception of the upper limbs in any species. We used fMRI adaptation to demonstrate dynamic hand-centered encoding of space by reporting response suppression in human premotor and posterior parietal cortices to repeated presentations of an object near the hand for different arm postures. Furthermore, we show that such spatial representation is related to changes in body perception, being remapped onto a prosthetic hand if perceived as ones own during an illusion. Interestingly, our results further suggest that peri-hand space remapping in the premotor cortex is most tightly linked to the subjective feeling of ownership of the seen limb, whereas remapping in the posterior parietal cortex closely reflects changes in the position sense of the arm. These findings identify the neural bases for dynamic hand-centered encoding of peripersonal space in humans and provide hitherto missing evidence for the link between the peri-hand representation of space and the perceived self-attribution and position of the upper limb.

Peripersonal Space and Body Schema: Two Labels for the Same Concept?

To sensibly interact with the environment, like when grasping objects and navigating through space, the brain needs to compute not only target- and environment-related inputs, but also the size and spatial location of the entire body as well as of its parts. The neuronal construction and dynamic updating throughout the entire life of this bodily representation, commonly termed body schema in the literature, appears essential for efficient motor control and skilful tool-use. Meanwhile, recent contributions to the study of spatial multisensory processing have identified the peripersonal space as a particular region surrounding the body that acts as an interface between the body and the environment, for defensive and/or purposeful actions toward objects. In addition, the peripersonal space features plastic properties following tool-use that largely overlap those originally ascribed to the body schema, and have been actually interpreted as reflecting changes in the body schema itself. Here we seek to provide operational definitions and neuronal bases for each of these concepts, questioning whether sufficient evidence exists for them to be considered as the two faces of the same coin.

fMRI Adaptation Reveals a Cortical Mechanism for the Coding of Space Near the Hand

Behavioral studies in humans and electrophysiological recordings in nonhuman primates have suggested the existence of a specific representation of the space immediately surrounding the body. In macaques, neurons that have visual receptive fields limited to a region of space close around a body part have been found in premotor and parietal areas. These cells are hypothesized to encode the location of external objects in coordinate systems that are centered on individual body parts. In the present study, we used an fMRI adaptation paradigm on healthy participants to reveal areas in the anterior part of the intraparietal sulcus, the inferior parietal lobe (supramarginal gyrus), and the dorsal and ventral portions of the premotor cortex that exhibit selective BOLD adaptation to an object moving near the right hand. Crucially, these areas did not manifest adaptation if the stimulus was presented in far space (100 cm) or when the hand was retracted from the object. This hand-centered selectivity could not be detected when a traditional fMRI analysis approach was used. These findings are important as they provide the most conclusive neuroimaging evidence to date for a representation of near-personal space in the human brain. They also demonstrate a selective mechanism implemented by human perihand neurons in the premotor and posterior parietal areas and add to earlier findings from humans and nonhuman primates.

Disintegration of Multisensory Signals from the Real Hand Reduces Default Limb Self-Attribution: An fMRI Study

The perception of our limbs in space is built upon the integration of visual, tactile, and proprioceptive signals. Accumulating evidence suggests that these signals are combined in areas of premotor, parietal, and cerebellar cortices. However, it remains to be determined whether neuronal populations in these areas integrate hand signals according to basic temporal and spatial congruence principles of multisensory integration. Here, we developed a setup based on advanced 3D video technology that allowed us to manipulate the spatiotemporal relationships of visuotactile (VT) stimuli delivered on a healthy human participants real hand during fMRI and investigate the ensuing neural and perceptual correlates. Our experiments revealed two novel findings. First, we found responses in premotor, parietal, and cerebellar regions that were dependent upon the spatial and temporal congruence of VT stimuli. This multisensory integration effect required a simultaneous match between the seen and felt postures of the hand, which suggests that congruent visuoproprioceptive signals from the upper limb are essential for successful VT integration. Second, we observed that multisensory conflicts significantly disrupted the default feeling of ownership of the seen real limb, as indexed by complementary subjective, psychophysiological, and BOLD measures. The degree to which self-attribution was impaired could be predicted from the attenuation of neural responses in key multisensory areas. These results elucidate the neural bases of the integration of multisensory hand signals according to basic spatiotemporal principles and demonstrate that the disintegration of these signals leads to “disownership” of the seen real hand.

Coding of Visual Space during Motor Preparation: Approaching Objects Rapidly Modulate Corticospinal Excitability in Hand-Centered Coordinates

Defensive behaviors, such as withdrawing your hand to avoid potentially harmful approaching objects, rely on rapid sensorimotor transformations between visual and motor coordinates. We examined the reference frame for coding visual information about objects approaching the hand during motor preparation. Subjects performed a simple visuomanual task while a task-irrelevant distractor ball rapidly approached a location either near to or far from their hand. After the distractor ball appearance, single pulses of transcranial magnetic stimulation were delivered over the subjects primary motor cortex, eliciting motor evoked potentials (MEPs) in their responding hand. MEP amplitude was reduced when the ball approached near the responding hand, both when the hand was on the left and the right of the midline. Strikingly, this suppression occurred very early, at 70–80 ms after ball appearance, and was not modified by visual fixation location. Furthermore, it was selective for approaching balls, since static visual distractors did not modulate MEP amplitude. Together with additional behavioral measurements, we provide converging evidence for automatic hand-centered coding of visual space in the human brain.

Grasping actions remap peripersonal space

The portion of space that closely surrounds our body parts is termed peripersonal space, and it has been shown to be represented in the brain through multisensory processing systems. Here, we tested whether voluntary actions, such as grasping an object, may remap such multisensory spatial representation. Participants discriminated touches on the hand they used to grasp an object containing task-irrelevant visual distractors. Compared with a static condition, reach-to-grasp movements increased the interference exerted by visual distractors over tactile targets. This remapping of multisensory space was triggered by action onset and further enhanced in real time during the early action execution phase. Additional experiments showed that this phenomenon is hand-centred. These results provide the first evidence of a functional link between voluntary object-oriented actions and multisensory coding of the space around us.

Multisensory Representation of the Space Near the Hand: From Perception to Action and Interindividual Interactions

When interacting with objects and other people, the brain needs to locate our limbs and the relevant visual information surrounding them. Studies on monkeys showed that information from different sensory modalities converge at the single cell level within a set of interconnected multisensory frontoparietal areas. It is largely accepted that this network allows for multisensory processing of the space surrounding the body (peripersonal space), whose function has been linked to the sensory guidance of appetitive and defensive movements, and localization of the limbs in space. In the current review, we consider multidisciplinary findings about the processing of the space near the hands in humans and offer a convergent view of its functions and underlying neural mechanisms. We will suggest that evolution has provided the brain with a clever tool for representing visual information around the hand, which takes the hand itself as a reference for the coding of surrounding visual space. We will contend that the hand-centered representation of space, known as perihand space, is a multisensory-motor interface that allows interaction with the objects and other persons around us.

Touch perception reveals the dominance of spatial over digital representation of numbers

We learn counting on our fingers, and the digital representation of numbers we develop is still present in adulthood [Andres M, et al. (2007) J Cognit Neurosci 19:563–576]. Such an anatomy–magnitude association establishes tight functional correspondences between fingers and numbers [Di Luca S, et al. (2006) Q J Exp Psychol 59:1648–1663]. However, it has long been known that small-to-large magnitude information is arranged left-to-right along a mental number line [Dehaene S, et al. (1993) J Exp Psychol Genet 122:371–396]. Here, we investigated touch perception to disambiguate whether number representation is embodied on the hand (“1” = thumb; “5” = little finger) or disembodied in the extrapersonal space (“1” = left; “5” = right). We directly contrasted these number representations in two experiments using a single centrally located effector (the foot) and a simple postural manipulation of the hand (palm-up vs. palm-down). We show that visual presentation of a number (“1” or “5”) shifts attention cross-modally, modulating the detection of tactile stimuli delivered on the little finger or thumb. With the hand resting palm-down, subjects perform better when reporting tactile stimuli delivered to the little finger after presentation of number “5” than number “1.” Crucially, this pattern reverses (better performance after number “1” than “5”) when the hand is in a palm-up posture, in which the position of the fingers in external space, but not their relative anatomical position, is reversed. The human brain can thus use either space- or body-based representation of numbers, but in case of competition, the former dominates the latter, showing the stronger role played by the mental number line organization.

Grab an object with a tool and change your body: tool-use-dependent changes of body representation for action

Along the evolutionary history, humans have reached a high level of sophistication in the way they interact with the environment. One important step in this process has been the introduction of tools, enabling humans to go beyond the boundaries of their physical possibilities. Here, we focus on some “low level” aspects of sensorimotor processing that highlight how tool-use plays a causal role in shaping body representations, an essential plastic feature for efficient motor control during development and skilful tool-use in the adult life. We assess the evidence supporting the hypothesis that tools are incorporated in body representation for action, which is the body schema, by critically reviewing some previous findings and providing new data from on-going work in our laboratory. In particular, we discuss several experiments that reveal the effects of tool-use both on the kinematics of hand movements and the localization of somatosensory stimuli on the body surface, as well as the conditions that are necessary for these effects to be manifested. We suggest that overall these findings speak in favour of genuine tool-use-dependent plasticity of the body representation for the control of action.