Implicit signatures of voluntary action reduce with repeated motor practice.

The sense of controlling one's actions and their consequences is a critical aspect of successful motor activity. While motor performance typically improves with learning, it is unclear whether, how, and why higher order aspects of motor cognition are also affected. Here, we used an implicit measure of sense of agency-the 'intentional binding' effect-as participants learned to make a skilled action involving precise control of thumb adduction. These actions were predictably followed by a tone (the outcome). At pre-test, we showed the perceived time of the tone was shifted towards the thumb action, compared to a control condition in which tones occurred without actions. Next, a relevant training group learned to refine the direction of the thumb movement, while an irrelevant training group was trained on another movement. Manipulation checks demonstrated that, as expected, the relevant training group improved performance of the trained movement, while the irrelevant training group did not. Critically, while both groups still showed binding of the tone towards the thumb action at post-test, the relevant training group showed less binding than the irrelevant training group. Given the link between intentional binding and volitional control of action, we suggest our result demonstrates subjective agency over the outcome of a skilled action decreases as practice makes the skilled action more fluent. We suggest that this reduction in sense of agency over movement outcomes is consistent with the decreasing cognitive engagement, or automatization, that occurs during skill learning.

Similar somatotopy for active and passive digit representation in primary somatosensory cortex.

Scientists traditionally use passive stimulation to examine the organisation of primary somatosensory cortex (SI). However, given the close, bidirectional relationship between the somatosensory and motor systems, active paradigms involving free movement may uncover alternative SI representational motifs. Here, we used 7 Tesla functional magnetic resonance imaging to compare hallmark features of SI digit representation between active and passive tasks which were unmatched on task or stimulus properties. The spatial location of digit maps, somatotopic organisation, and inter-digit representational structure were largely consistent between tasks, indicating representational consistency. We also observed some task differences. The active task produced higher univariate activity and multivariate representational information content (inter-digit distances). The passive task showed a trend towards greater selectivity for digits versus their neighbours. Our findings highlight that, while the gross features of SI functional organisation are task invariant, it is important to also consider motor contributions to digit representation.

Malleability of the cortical hand map following a finger nerve block.

Electrophysiological studies in monkeys show that finger amputation triggers local remapping within the deprived primary somatosensory cortex (S1). Human neuroimaging research, however, shows persistent S1 representation of the missing hand's fingers, even decades after amputation. Here, we explore whether this apparent contradiction stems from underestimating the distributed peripheral and central representation of fingers in the hand map. Using pharmacological single-finger nerve block and 7-tesla neuroimaging, we first replicated previous accounts (electrophysiological and other) of local S1 remapping. Local blocking also triggered activity changes to nonblocked fingers across the entire hand area. Using methods exploiting interfinger representational overlap, however, we also show that the blocked finger representation remained persistent despite input loss. Computational modeling suggests that both local stability and global reorganization are driven by distributed processing underlying the topographic map, combined with homeostatic mechanisms. Our findings reveal complex interfinger representational features that play a key role in brain (re)organization, beyond (re)mapping.

Interplay of tactile and motor information in constructing spatial self-perception.

During active movement, there is normally a tight relation between motor command and sensory representation about the resulting spatial displacement of the body. Indeed, some theories of space perception emphasize the topographic layout of sensory receptor surfaces, while others emphasize implicit spatial information provided by the intensity of motor command signals. To identify which has the primary role in spatial perception, we developed experiments based on everyday self-touch, in which the right hand strokes the left arm. We used a robot-mediated form of self-touch to decouple the spatial extent of active or passive right hand movements from their tactile consequences. Participants made active movements of the right hand between unpredictable, haptically defined start and stop positions, or the hand was passively moved between the same positions. These movements caused a stroking tactile motion by a brush along the left forearm, with minimal delay, but with an unpredictable spatial gain factor. Participants judged the spatial extent of either the right hand's movement, or of the resulting tactile stimulation to their left forearm. Across five experiments, we found that movement extent strongly interfered with tactile extent perception, and vice versa. Crucially, interference in both directions was stronger during active than passive movements. Thus, voluntary motor commands produced stronger integration of multiple sensorimotor signals underpinning the perception of personal space. Our results prompt a reappraisal of classical theories that reduce space perception to motor command information.

Human perceptual learning is delayed by the N-methyl-D-aspartate receptor partial agonist D-cycloserine.

BACKGROUND: The optimisation of learning has long been a focus of scientific research, particularly in relation to improving psychological treatment and recovery of brain function. Previously, partial N-methyl-D-aspartate agonists have been shown to augment reward learning, procedural learning and psychological therapy, but many studies also report no impact of these compounds on the same processes. AIMS: Here we investigate whether administration of an N-methyl-D-aspartate partial agonist (D-cycloserine) modulates a previously unexplored process - tactile perceptual learning. Further, we use a longitudinal design to investigate whether N-methyl-D-aspartate-related learning effects vary with time, thereby providing a potentially simple explanation for apparent mixed effects in previous research. METHODS: Thirty-four volunteers were randomised to receive one dose of 250 mg D-cycloserine or placebo 2 h before tactile sensitivity training. Tactile perception was measured using psychophysical methods before and after training, and 24/48 h later. RESULTS: The placebo group showed immediate within-day tactile perception gains, but no further improvements between-days. In contrast, tactile perception remained at baseline on day one in the D-cycloserine group (no within-day learning), but showed significant overnight gains on day two. Both groups were equivalent in tactile perception by the final testing - indicating N-methyl-D-aspartate effects changed the timing, but not the overall amount of tactile learning. CONCLUSIONS: In sum, we provide first evidence for modulation of perceptual learning by administration of a partial N-methyl-D-aspartate agonist. Resolving how the effects of such compounds become apparent over time will assist the optimisation of testing schedules, and may help resolve discrepancies across the learning and cognition domains.

Organized Toe Maps in Extreme Foot Users.

Although the fine-grained features of topographic maps in the somatosensory cortex can be shaped by everyday experience, it is unknown whether behavior can support the expression of somatotopic maps where they do not typically occur. Unlike the fingers, represented in all primates, individuated toe maps have only been found in non-human primates. Using 1-mm resolution fMRI, we identify organized toe maps in two individuals born without either upper limb who use their feet to substitute missing hand function and even support their profession as foot artists. We demonstrate that the ordering and structure of the artists' toe representation mimics typical hand representation. We further reveal "hand-like" features of activity patterns, not only in the foot area but also similarly in the missing hand area. We suggest humans may have an innate capacity for forming additional topographic maps that can be expressed with appropriate experience.

Blocking tactile input to one finger using anaesthetic enhances touch perception and learning in other fingers.

Brain plasticity is a key mechanism for learning and recovery. A striking example of plasticity in the adult brain occurs following input loss, for example, following amputation, whereby the deprived zone is "invaded" by new representations. Although it has long been assumed that such reorganization leads to functional benefits for the invading representation, the behavioral evidence is controversial. Here, we investigate whether a temporary period of somatosensory input loss to one finger, induced by anesthetic block, is sufficient to cause improvements in touch perception ("direct" effects of deafferentation). Further, we determine whether this deprivation can improve touch perception by enhancing sensory learning processes, for example, by training ("interactive" effects). Importantly, we explore whether direct and interactive effects of deprivation are dissociable by directly comparing their effects on touch perception. Using psychophysical thresholds, we found brief deprivation alone caused improvements in tactile perception of a finger adjacent to the blocked finger but not to non-neighboring fingers. Two additional groups underwent minimal tactile training to one finger either during anesthetic block of the neighboring finger or a sham block with saline. Deprivation significantly enhanced the effects of tactile perceptual training, causing greater learning transfer compared with sham block. That is, following deafferentation and training, learning gains were seen in fingers normally outside the boundaries of topographic transfer of tactile perceptual learning. Our results demonstrate that sensory deprivation can improve perceptual abilities, both directly and interactively, when combined with sensory learning. This dissociation provides novel opportunities for future clinical interventions to improve sensation. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Obtaining and maintaining cortical hand representation as evidenced from acquired and congenital handlessness.

A key question in neuroscience is how cortical organisation relates to experience. Previously we showed that amputees experiencing highly vivid phantom sensations maintain cortical representation of their missing hand (Kikkert et al., 2016). Here, we examined the role of sensory hand experience on persistent hand representation by studying individuals with acquired and congenital hand loss. We used representational similarity analysis in primary somatosensory and motor cortex during missing and intact hand movements. We found that key aspects of acquired amputees' missing hand representation persisted, despite varying vividness of phantom sensations. In contrast, missing hand representation of congenital one-handers, who do not experience phantom sensations, was significantly reduced. Across acquired amputees, individuals' reported motor control over their phantom hand positively correlated with the extent to which their somatosensory hand representation was normally organised. We conclude that once cortical organisation is formed, it is remarkably persistent, despite long-term attenuation of peripheral signals.

Handedness modulates proprioceptive drift in the rubber hand illusion.

Preference for use of either the left or right hand ('handedness') has been linked with modulations of perception and sensory processing-both of space and the body. Here we ask whether multisensory integration of bodily information also varies as a function of handedness. We created a spatial disparity between visual and somatosensory hand position information using the rubber hand illusion, and use the magnitude of illusory shifts in hand position (proprioceptive 'drift') as a tool to probe the weighted integration of multisensory information. First, we found drift was significantly reduced when the illusion was performed on the dominant vs. non-dominant hand. We suggest increased manual dexterity of the dominant hand causes greater representational stability and thus an increased resistance to bias by the illusion induction. Second, drift was generally greatest when the hand was in its habitual action space (i.e., near the shoulder of origin), compared to when it laterally displaced towards, or across the midline. This linear effect, however, was only significant for the dominant hand-in both left- and right-handed groups. Thus, our results reveal patterns of habitual hand action modulate drift both within a hand (drift varies with proximity to action space), and between hands (differences in drift between the dominant and non-dominant hands). In contrast, we were unable to find conclusive evidence to support, or contradict, an overall difference between left- and right-handers in susceptibility to RHI drift (i.e., total drift, collapsed across hand positions). In sum, our results provide evidence that patterns of daily activity-and the subsequent patterns of sensory input-shape multisensory integration across space.

Enhanced integration of multisensory body information by proximity to "habitual action space".

Previous research suggests integration of visual and somatosensory inputs is enhanced within reaching (peripersonal) space. In such experiments, somatosensory inputs are presented on the body while visual inputs are moved relatively closer to, or further from the body. It is unclear, therefore, whether enhanced integration in "peripersonal space" is truly due to proximity of visual inputs to the body space, or, simply the distance between the inputs (which also affects integration). Using a modified induction of the rubber hand illusion, here we measured proprioceptive drift as an index of visuosomatosensory integration when distance between the two inputs was constrained, and absolute distance from the body was varied. Further, we investigated whether integration varies with proximity of inputs to the habitual action space of the arm-rather than the actual arm itself. In Experiment 1, integration was enhanced with inputs proximal to habitual action space, and reduced with lateral distance from this space. This was not attributable to an attentional or perceptual bias of external space because the pattern of proprioceptive drift was opposite for left and right hand illusions, that is, consistently maximal at the shoulder of origin (Experiment 2). We conclude that habitual patterns of action modulate visuosomatosensory integration. It appears multisensory integration is modulated in locations of space that are functionally relevant for behavior, whether an actual body part resides within that space or not. (PsycINFO Database Record

Transfer of tactile perceptual learning to untrained neighboring fingers reflects natural use relationships.

Tactile learning transfers from trained to untrained fingers in a pattern that reflects overlap between the representations of fingers in the somatosensory system (e.g., neurons with multifinger receptive fields). While physical proximity on the body is known to determine the topography of somatosensory representations, tactile coactivation is also an established organizing principle of somatosensory topography. In this study we investigated whether tactile coactivation, induced by habitual inter-finger cooperative use (use pattern), shapes inter-finger overlap. To this end, we used psychophysics to compare the transfer of tactile learning from the middle finger to its adjacent fingers. This allowed us to compare transfer to two fingers that are both physically and cortically adjacent to the middle finger but have differing use patterns. Specifically, the middle finger is used more frequently with the ring than with the index finger. We predicted this should lead to greater representational overlap between the former than the latter pair. Furthermore, this difference in overlap should be reflected in differential learning transfer from the middle to index vs. ring fingers. Subsequently, we predicted temporary learning-related changes in the middle finger's representation (e.g., cortical magnification) would cause transient interference in perceptual thresholds of the ring, but not the index, finger. Supporting this, longitudinal analysis revealed a divergence where learning transfer was fast to the index finger but relatively delayed to the ring finger. Our results support the theory that tactile coactivation patterns between digits affect their topographic relationships. Our findings emphasize how action shapes perception and somatosensory organization.

Higher-order cognitive factors affect subjective but not proprioceptive aspects of self-representation in the rubber hand illusion.

In the current study we look at whether subjective and proprioceptive aspects of selfrepresentation are separable components subserved by distinct systems of multisensory integration. We used the rubber hand illusion (RHI) to draw the location of the 'self' away from the body, towards extracorporeal space (Out Condition), thereby violating top-down information about the body location. This was compared with the traditional RHI which drew position of the 'self' towards the body (In Condition). We were successfully able to draw proprioceptive position of the limbs in and out from the body suggesting body perception is a purely bottom-up process, resistant to top-down effects. Conversely, we found subjective self-representation was altered by the violation of top-down body information - as the strong association of subjective and proprioceptive factors found in the In Condition became non-significant in the Out Condition. Interestingly, we also found evidence that subjective embodiment can modulate tactile perception.