Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination.

From observations in rodents, it has been suggested that the cellular basis of learning-dependent changes, detected using structural MRI, may be increased dendritic spine density, alterations in astrocyte volume, and adaptations within intracortical myelin. Myelin plasticity is crucial for neurological function, and active myelination is required for learning and memory. However, the dynamics of myelin plasticity and how it relates to morphometric-based measurements of structural plasticity remains unknown. We used a motor skill learning paradigm in male mice to evaluate experience-dependent brain plasticity by voxel-based morphometry (VBM) in longitudinal MRI, combined with a cross-sectional immunohistochemical investigation. Whole-brain VBM revealed nonlinear decreases in gray matter volume (GMV) juxtaposed to nonlinear increases in white matter volume (WMV) within GM that were best modeled by an asymptotic time course. Using an atlas-based cortical mask, we found nonlinear changes with learning in primary and secondary motor areas and in somatosensory cortex. Analysis of cross-sectional myelin immunoreactivity in forelimb somatosensory cortex confirmed an increase in myelin immunoreactivity followed by a return towards baseline levels. Further investigations using quantitative confocal microscopy confirmed these changes specifically to the length density of myelinated axons. The absence of significant histological changes in cortical thickness suggests that nonlinear morphometric changes are likely due to changes in intracortical myelin for which morphometric WMV in somatosensory cortex significantly correlated with myelin immunoreactivity. Together, these observations indicate a nonlinear increase of intracortical myelin during learning and support the hypothesis that myelin is a component of structural changes observed by VBM during learning.

Tool use and language share syntactic processes and neural patterns in the basal ganglia.

Does tool use share syntactic processes with language? Acting with a tool is thought to add a hierarchical level into the motor plan. In the linguistic domain, syntax is the cognitive function handling interdependent elements. Using functional magnetic resonance imaging, we detected common neurofunctional substrates in the basal ganglia subserving both tool use and syntax in language. The two abilities elicited similar patterns of neural activity, indicating the existence of shared functional resources. Manual actions and verbal working memory did not contribute to this common network. Consistent with the existence of shared neural resources, we observed bidirectional behavioral enhancement of tool use and syntactic skills in language so that training one function improves performance in the other. This reveals supramodal syntactic processes for tool use and language.

Me, you, and our object: Peripersonal space recruitment during executed and observed actions depends on object ownership.

Peripersonal space (PPS) is a spatial representation that codes objects close to one's own and to someone else's body in a multisensory-motor frame of reference to support appropriate motor behavior. Recent theories framed PPS beyond its original sensorimotor aspects and proposed to relate it to social aspects of the self. Here, we manipulated the ownership status of an object ("whose object this is") to test the sensitivity of PPS to such a pervasive aspect of society. To this aim, we assessed PPS through a well-established visuo-tactile task within a novel situation where we had dyads of participants either grasping or observing to grasp an object, whose ownership was experimentally assigned to either participant (individual ownership), or to both participants (shared ownership). When ownership was assigned exclusively ("this belongs to you/the other," Experiment 1), the PPS recruitment emerged when grasping one's own object (I grasp my object), as well as when observing others grasping their own object (you grasp your object). Instead, no PPS effect was found when grasping (and observing to grasp) an object that was not one's own (I grasp yours, you grasp mine). When ownership was equally assigned ("this belongs to both of you," Experiment 2), a similar PPS recruitment emerged and, again, both when the action toward the shared object was executed and merely observed. These findings reveal that ownership is critical in shaping relatively low-level aspects of body-object interactions during everyday simple actions, highlighting the deep mark of ownership over social behavior. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Language as a Tool: Motor Proficiency Using a Tool Predicts Individual Linguistic Abilities.

Different disciplines converge to trace language evolution from motor skills. The human ability to use tools has been advocated as a fundamental step toward the emergence of linguistic processes in the brain. Neuropsychological and neuroimaging research has established that linguistic functions and tool-use are mediated by partially overlapping brain networks. Yet, scholars still theoretically debate whether the relationship between tool-use and language is contingent or functionally relevant, since empirical evidence is critically missing. Here, we measured both linguistic production and tool-use abilities in the same participants, as well as manual and linguistic motor skills. A path analysis ruling out unspecific contributions from manual or linguistic motor skills, showed that motor proficiency using a tool lawfully predicts differences in individual linguistic production. In addition, more complex tool-use reveals stronger association between linguistic production and tool mastery. These findings establish the existence of shared cognitive processes between tool-use and language.

Aim and Plausibility of Action Chains Remap Peripersonal Space.

Successful interaction with objects in the peripersonal space requires that the information relative to current and upcoming positions of our body is continuously monitored and updated with respect to the location of target objects. Voluntary actions, for example, are known to induce an anticipatory remapping of the peri-hand space (PHS, i.e., the space near the acting hand) during the very early stages of the action chain: planning and initiating an object grasp increase the interference exerted by visual stimuli coming from the object on touches delivered to the grasping hand, thus allowing for hand-object position monitoring and guidance. Voluntarily grasping an object, though, is rarely performed in isolation. Grasping a candy, for example, is most typically followed by concatenated secondary action steps (bringing the candy to the mouth and swallowing it) that represent the agent's ultimate intention (to eat the candy). However, whether and when complex action chains remap the PHS remains unknown, just as whether remapping is conditional to goal achievability (e.g., candy-mouth fit). Here we asked these questions by assessing changes in visuo-tactile interference on the acting hand while participants had to grasp an object serving as a support for an elongated candy, and bring it toward their mouth. Depending on its orientation, the candy could potentially enter the participants' mouth (plausible goal), or not (implausible goal). We observed increased visuo-tactile interference at relatively late stages of the action chain, after the object had been grasped, and only when the action goal was plausible. These findings suggest that multisensory interactions during action execution depend upon the final aim and plausibility of complex goal-directed actions, and extend our knowledge about the role of peripersonal space in guiding goal-directed voluntary actions.

Action Planning Modulates Peripersonal Space.

Peripersonal space is a multisensory representation relying on the processing of tactile and visual stimuli presented on and close to different body parts. The most studied peripersonal space representation is perihand space (PHS), a highly plastic representation modulated following tool use and by the rapid approach of visual objects. Given these properties, PHS may serve different sensorimotor functions, including guidance of voluntary actions such as object grasping. Strong support for this hypothesis would derive from evidence that PHS plastic changes occur before the upcoming movement rather than after its initiation, yet to date, such evidence is scant. Here, we tested whether action-dependent modulation of PHS, behaviorally assessed via visuotactile perception, may occur before an overt movement as early as the action planning phase. To do so, we probed tactile and visuotactile perception at different time points before and during the grasping action. Results showed that visuotactile perception was more strongly affected during the planning phase (250 msec after vision of the target) than during a similarly static but earlier phase (50 msec after vision of the target). Visuotactile interaction was also enhanced at the onset of hand movement, and it further increased during subsequent phases of hand movement. Such a visuotactile interaction featured interference effects during all phases from action planning onward as well as a facilitation effect at the movement onset. These findings reveal that planning to grab an object strengthens the multisensory interaction of visual information from the target and somatosensory information from the hand. Such early updating of the visuotactile interaction reflects multisensory processes supporting motor planning of actions.

Expansion and Renormalization of Human Brain Structure During Skill Acquisition.

Research on human brain changes during skill acquisition has revealed brain volume expansion in task-relevant areas. However, the large number of skills that humans acquire during ontogeny militates against plasticity as a perpetual process of volume growth. Building on animal models and available theories, we promote the expansion-renormalization model for plastic changes in humans. The model predicts an initial increase of gray matter structure, potentially reflecting growth of neural resources like neurons, synapses, and glial cells, which is followed by a selection process operating on this new tissue leading to a complete or partial return to baseline of the overall volume after selection has ended. The model sheds new light on available evidence and current debates and fosters the search for mechanistic explanations.

Proprioception Is Necessary for Body Schema Plasticity: Evidence from a Deafferented Patient.

The ability of using a large variety of tools is important in our daily life. Behind human tool-use abilities lays the brain capacity to incorporate tools into the body representation for action (Body Schema, BS), thought to rely mainly on proprioceptive information. Here, we tested whether tool incorporation is possible in absence of proprioception by studying a patient with right upper-limb deafferentation. We adopted a paradigm sensitive to changes of the BS and analyzed the kinematics of free-hand movements before and after tool-use, in three sessions over a period of 2 years. In the first session, before tool-use, the kinematics of the deafferented hand was disrupted. Similarly, the first movements with the tool (a mechanical grabber elongating the arm by ~40 cm) showed an abnormal profile that tended to normalize at the end of the session. Subsequent free-hand movements were also normalized. At session 2, 6 months later, the patient exhibited normal free-hand kinematic profiles, additionally showing changes in grasping kinematics after tool-use, but no sign of tool incorporation. A follow-up 2 years later, further confirmed the normalized kinematic profile but the absence of tool incorporation. This first description of tool-use in absence of proprioception shows the fundamental role of proprioception in the update of the BS. These results provide an important further step in understanding human motor control and have implications for future development of rehabilitation programs for patients with sensory deficits.

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.

A shared representation of the space near oneself and others in the human premotor cortex.

Interactions between people require shared high-level cognitive representations of action goals, intentions, and mental states, but do people also share their representation of space? The human ventral premotor (PMv) and parietal cortices contain neuronal populations coding for the execution and observation of actions, analogous to the mirror neurons identified in monkeys. This neuronal system is tuned to the location of the acting person relative to the observer and the target of the action. Therefore, it can be theorized that the observer's brain constructs a low-level, body-centered representation of the space around others similar to one's own peripersonal space representation. Single-cell recordings have reported that parietal visuotactile neurons discharge for objects near specific parts of a monkey's own body and near the corresponding body parts of another individual. In humans, no neuroimaging study has investigated this issue. Here, we identified neuronal populations in the human PMv that encode the space near both one's own hand and another person's hand. The shared peripersonal space representation could support social interactions by coding sensory events, actions, and cognitive processes in a common spatial reference frame.

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 participant's 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.

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 one's 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.

Keeping the world at hand: rapid visuomotor processing for hand-object interactions.

The existence of hand-centred visual processing has long been established in the macaque premotor cortex. These hand-centred mechanisms have been thought to play some general role in the sensory guidance of movements towards objects, or, more recently, in the sensory guidance of object avoidance movements. We suggest that these hand-centred mechanisms play a specific and prominent role in the rapid selection and control of manual actions following sudden changes in the properties of the objects relevant for hand-object interactions. We discuss recent anatomical and physiological evidence from human and non-human primates, which indicates the existence of rapid processing of visual information for hand-object interactions. This new evidence demonstrates how several stages of the hierarchical visual processing system may be bypassed, feeding the motor system with hand-related visual inputs within just 70 ms following a sudden event. This time window is early enough, and this processing rapid enough, to allow the generation and control of rapid hand-centred avoidance and acquisitive actions, for aversive and desired objects, respectively.

Neglect: a multisensory deficit?

Neglect is a neurological syndrome characterised by a lack of conscious perception of events localised in the contralesional side of space. Here, we consider the possible multisensory nature of this disorder, critically reviewing the literature devoted to multisensory manifestations and processing in neglect. Although its most striking manifestations have been observed in the visual domain, a number of studies demonstrate that neglect can affect virtually any sensory modality, in particular touch and audition. Furthermore, a few recent studies have reported a correlation in severity between visual and non-visual neglect-related deficits evaluated in the same patients, providing some preliminary support for a multisensory conception of neglect. Sensory stimulation and sensorimotor adaptation techniques, aimed at alleviating neglect, have also been shown to affect several sensory modalities, including some that were not directly affected by the intervention. Finally, in some cases neglect can bias multisensory interactions known to occur in healthy individuals, leading to abnormal behaviour or uncovering multisensory compensation mechanisms. This evidence, together with neurophysiological and neuroimaging data revealing the multisensory role played by the areas that are most commonly damaged in neglect patients, seems to speak in favour of neglect as a multisensory disorder. However, since most previous studies were not conducted with the specific purpose of systematically investigating the multisensory nature of neglect, we conclude that more research is needed to appropriately assess this question, and suggest some methodological guidelines that we hope will help clarify this issue. At present, the conception of neglect as a multisensory disorder remains a promising working hypothesis that may help define the pathophysiology of this syndrome.

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.

Studying Multisensory Processing and Its Role in the Representation of Space through Pathological and Physiological Crossmodal Extinction.

The study of crossmodal extinction has brought a considerable contribution to our understanding of how the integration of stimuli perceived in multiple sensory modalities is used by the nervous system to build coherent representations of the space that directly surrounds us. Indeed, by revealing interferences between stimuli in a disturbed system, extinction provides an invaluable opportunity to investigate the interactions that normally exist between those stimuli in an intact system. Here, we first review studies on pathological crossmodal extinction, from the original demonstration of its existence, to its role in the exploration of the multisensory neural representation of space and the current theoretical accounts proposed to explain the mechanisms involved in extinction and multisensory competition. Then, in the second part of this paper, we report recent findings showing that physiological multisensory competition phenomena resembling clinical crossmodal extinction exist in the healthy brain. We propose that the development of a physiological model of sensory competition is fundamental to deepen our understanding of the cerebral mechanisms of multisensory perception and integration. In addition, a similar approach to develop a model of physiological sensory competition in non-human primates should allow combining functional neuroimaging with more invasive techniques, such as transient focal lesions, in order to bridge the gap between works done in the two species and at different levels of analysis.

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.

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 subject's 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.