Touch localization after nerve repair in the hand: insights from a new measurement tool.

Errors of touch localization after hand nerve injuries are common, and their measurement is important for evaluating functional recovery. Available empirical accounts have significant methodological limitations, however, and a quantitatively rigorous and detailed description of touch localization in nerve injury is lacking. Here, we develop a new method of measuring touch localization and evaluate its value for use in nerve injury. Eighteen patients with transection injuries to the median/ulnar nerves and 33 healthy controls were examined. The hand was blocked from the participant's view and points were marked on the volar surface using an ultraviolet (UV) pen. These points served as targets for touch stimulation. Two photographs were taken, one with and one without UV lighting, rendering targets seen and unseen, respectively. The experimenter used the photograph with visible targets to register their locations, and participants reported the felt position of each stimulation on the photograph with unseen targets. The error of localization and its directional components were measured, separate from misreferrals-errors made across digits, or from a digit to the palm. Nerve injury was found to significantly increase the error of localization. These effects were specific to the territory of the repaired nerve and showed considerable variability at the individual level, with some patients showing no evidence of impairment. A few patients also made abnormally high numbers of misreferrals, and the pattern of misreferrals in patients differed from that observed in healthy controls.NEW & NOTEWORTHY We provide a more rigorous and comprehensive account of touch localization in nerve injury than previously available. Our results show that touch localization is significantly impaired following median/ulnar nerve transection injuries and that these impairments are specific to the territory of the repaired nerve(s), vary considerably between patients, and can involve frequent errors spanning between digits.

Hand choice is unaffected by high frequency continuous theta burst transcranial magnetic stimulation to the posterior parietal cortex.

The current study used a high frequency TMS protocol known as continuous theta burst stimulation (cTBS) to test a model of hand choice that relies on competing interactions between the hemispheres of the posterior parietal cortex. Based on the assumption that cTBS reduces cortical excitability, the model predicts a significant decrease in the likelihood of selecting the hand contralateral to stimulation. An established behavioural paradigm was used to estimate hand choice in each individual, and these measures were compared across three stimulation conditions: cTBS to the left posterior parietal cortex, cTBS to the right posterior parietal cortex, or sham cTBS. Our results provide no supporting evidence for the interhemispheric competition model. We find no effects of cTBS on hand choice, independent of whether the left or right posterior parietal cortex was stimulated. Our results are nonetheless of value as a point of comparison against prior brain stimulation findings that, in contrast, provide evidence for a causal role for the posterior parietal cortex in hand choice.

Corrigendum: Changes in primary somatosensory cortex following allogeneic hand transplantation or autogenic hand replantation.

[This corrects the article DOI: 10.3389/fnimg.2022.919694.].

Interhemispheric transfer of post-amputation cortical plasticity within the human somatosensory cortex.

Animal models reveal that deafferenting forelimb injuries precipitate reorganization in both contralateral and ipsilateral somatosensory cortices. The functional significance and duration of these effects are unknown, and it is unclear whether they also occur in injured humans. We delivered cutaneous stimulation during functional magnetic resonance imaging (fMRI) to map the sensory cortical representation of the intact hand and lower face in a group of chronic, unilateral, upper extremity amputees (N = 19) and healthy matched controls (N = 29). Amputees exhibited greater activity than controls within the deafferented former sensory hand territory (S1f) during stimulation of the intact hand, but not of the lower face. Despite this cortical reorganization, amputees did not differ from controls in tactile acuity on their intact hands. S1f responses during hand stimulation were unrelated to tactile acuity, pain, prosthesis usage, or time since amputation. These effects appeared specific to the deafferented somatosensory modality, as fMRI visual mapping paradigm failed to detect any differences between groups. We conclude that S1f becomes responsive to cutaneous stimulation of the intact hand of amputees, and that this modality-specific reorganizational change persists for many years, if not indefinitely. The functional relevance of these changes, if any, remains unknown.

Active Haptic Perception in Robots: A Review.

In the past few years a new scenario for robot-based applications has emerged. Service and mobile robots have opened new market niches. Also, new frameworks for shop-floor robot applications have been developed. In all these contexts, robots are requested to perform tasks within open-ended conditions, possibly dynamically varying. These new requirements ask also for a change of paradigm in the design of robots: on-line and safe feedback motion control becomes the core of modern robot systems. Future robots will learn autonomously, interact safely and possess qualities like self-maintenance. Attaining these features would have been relatively easy if a complete model of the environment was available, and if the robot actuators could execute motion commands perfectly relative to this model. Unfortunately, a complete world model is not available and robots have to plan and execute the tasks in the presence of environmental uncertainties which makes sensing an important component of new generation robots. For this reason, today's new generation robots are equipped with more and more sensing components, and consequently they are ready to actively deal with the high complexity of the real world. Complex sensorimotor tasks such as exploration require coordination between the motor system and the sensory feedback. For robot control purposes, sensory feedback should be adequately organized in terms of relevant features and the associated data representation. In this paper, we propose an overall functional picture linking sensing to action in closed-loop sensorimotor control of robots for touch (hands, fingers). Basic qualities of haptic perception in humans inspire the models and categories comprising the proposed classification. The objective is to provide a reasoned, principled perspective on the connections between different taxonomies used in the Robotics and human haptic literature. The specific case of active exploration is chosen to ground interesting use cases. Two reasons motivate this choice. First, in the literature on haptics, exploration has been treated only to a limited extent compared to grasping and manipulation. Second, exploration involves specific robot behaviors that exploit distributed and heterogeneous sensory data.

Grasping with a new hand: Improved performance and normalized grasp-selective brain responses despite persistent functional changes in primary motor cortex and low-level sensory and motor impairments.

Hand loss can now be reversed through surgical transplantation years or decades after amputation. Remarkably, these patients come to use their new hand to skilfully grasp and manipulate objects. The brain mechanisms that make this possible are unknown. Here we test the hypothesis that the anterior intraparietal cortex (aIPC) - a multimodal region implicated in hand preshaping and error correction during grasping - plays a key role in this compensatory grasp control. Motion capture and fMRI are used to characterize hand kinematics and brain responses during visually guided grasping with a transplanted hand at 26 and 41 months post-transplant in patient DR, a former hand amputee of 13 years. Compared with matched controls, DR shows increasingly normal grasp kinematics paralleled by increasingly robust grasp-selective fMRI responses within the very same brain areas that show grasp-selectivity in controls, including the aIPC, premotor and cerebellar cortices. Paradoxically, over this same time DR exhibits significant limitations in basic sensory and motor functions, and persistent amputation-related functional reorganization of primary motor cortex. Movements of the non-transplanted hand positively activate the ipsilateral primary motor hand area - a functional marker of persistent interhemispheric amputation-related reorganization. Our data demonstrate for the first time that even after more than a decade of living as an amputee the normative functional brain organization governing the control of grasping can be restored. We propose that the aIPC and interconnected premotor and cerebellar cortices enable grasp normalization by compensating for the functional impact of reorganizational changes in primary sensorimotor cortex and targeting errors in regenerating peripheral nerves.

Psychophysical and neuroimaging responses to moving stimuli in a patient with the Riddoch phenomenon due to bilateral visual cortex lesions.

Patients with injury to early visual cortex or its inputs can display the Riddoch phenomenon: preserved awareness for moving but not stationary stimuli. We provide a detailed case report of a patient with the Riddoch phenomenon, MC. MC has extensive bilateral lesions to occipitotemporal cortex that include most early visual cortex and complete blindness in visual field perimetry testing with static targets. Nevertheless, she shows a remarkably robust preserved ability to perceive motion, enabling her to navigate through cluttered environments and perform actions like catching moving balls. Comparisons of MC's structural magnetic resonance imaging (MRI) data to a probabilistic atlas based on controls reveals that MC's lesions encompass the posterior, lateral, and ventral early visual cortex bilaterally (V1, V2, V3A/B, LO1/2, TO1/2, hV4 and VO1 in both hemispheres) as well as more extensive damage to right parietal (inferior parietal lobule) and left ventral occipitotemporal cortex (VO1, PHC1/2). She shows some sparing of anterior occipital cortex, which may account for her ability to see moving targets beyond ~15 degrees eccentricity during perimetry. Most strikingly, functional and structural MRI revealed robust and reliable spared functionality of the middle temporal motion complex (MT+) bilaterally. Moreover, consistent with her preserved ability to discriminate motion direction in psychophysical testing, MC also shows direction-selective adaptation in MT+. A variety of tests did not enable us to discern whether input to MT+ was driven by her spared anterior occipital cortex or subcortical inputs. Nevertheless, MC shows rich motion perception despite profoundly impaired static and form vision, combined with clear preservation of activation in MT+, thus supporting the role of MT+ in the Riddoch phenomenon.

Now and then: Hand choice is influenced by recent action history.

Action choices are influenced by recent past and predicted future action states. Here, we demonstrate that recent hand-choice history affects both current hand choices and response times to initiate actions. Participants reach to contact visible targets using one hand. Hand choice is biased in favour of which hand was used recently, in particular, when the biomechanical costs of responding with either hand are similar, and repeated choices lead to reduced response times. These effects are also found to positively correlate. Participants who show strong effects of recent history on hand choice also tend to show strong effects of recent history on response times. The data are consistent with a computational efficiency interpretation whereby repeated action choices confer computational gains in the efficiency of underpinning processes. We discuss our results within the framework of this model, and with respect to balancing predicted gains and losses, and speculate about the possible underlying mechanisms in neural terms.

The neural basis of hand choice: An fMRI investigation of the Posterior Parietal Interhemispheric Competition model.

The current study investigates a new neurobiological model of human hand choice: The Posterior Parietal Interhemispheric Competition (PPIC) model. The model specifies that neural populations in bilateral posterior intraparietal and superior parietal cortex (pIP-SPC) encode actions in hand-specific terms, and compete for selection across and within hemispheres. Actions with both hands are encoded bilaterally, but the contralateral hand is overrepresented. We use a novel fMRI paradigm to test the PPIC model. Participants reach to visible targets while in the scanner, and conditions involving free choice of which hand to use (Choice) are compared with when hand-use is instructed. Consistent with the PPIC model, bilateral pIP-SPC is preferentially responsive for the Choice condition, and for actions made with the contralateral hand. In the right pIP-SPC, these effects include anterior intraparietal and superior parieto-occipital cortex. Left dorsal premotor cortex, and an area in the right lateral occipitotemporal cortex show the same response pattern, while the left inferior parietal lobule is preferentially responsive for the Choice condition and when using the ipsilateral hand. Behaviourally, hand choice is biased by target location - for targets near the left/right edges of the display, the hand in ipsilateral hemispace is favoured. Moreover, consistent with a competitive process, response times are prolonged for choices to more ambiguous targets, where hand choice is relatively unbiased, and fMRI responses in bilateral pIP-SPC parallel this pattern. Our data provide support for the PPIC model, and reveal a selective network of brain areas involved in free hand choice, including bilateral posterior parietal cortex, left-lateralized inferior parietal and dorsal premotor cortices, and the right lateral occipitotemporal cortex.

Contributions of the parietal cortex to increased efficiency of planning-based action selection.

Response selection is foundational to adaptive behavior, and considerable attention has been devoted to investigating this behavior under conditions in which the mapping between stimuli and responses is fixed. Results from prior studies implicate the left supramarginal gyrus (SMg), premotor and prefrontal cortices, as well as the cerebellum in this essential function. Yet, many goal-directed motor behaviors have multiple solutions with flexible mappings between stimuli and responses whose solutions are believed to involve prospective planning. Studies of selection under conditions of flexible mappings also reveal involvement of the left SMg, as well as bilateral premotor, superior parietal cortex (SPL) and pre-supplementary motor (pre-SMA) cortices, along with the cerebellum. This evidence is, however, limited by exclusive reliance on tasks that involve selection in the absence of overt action execution and without complete control of possible confounding effects related to differences in stimulus and response processing demands. Here, we address this limitation through use of a novel fMRI repetition suppression (FMRI-RS) paradigm. In our prime-probe design, participants select and overtly pantomime manual object rotation actions when the relationship between stimuli and responses is either flexible (experimental condition) or fixed (control condition). When trials were repeated in prime-probe pairs of the experimental condition, we detected improvements in performance accompanied by a significant suppression of blood oxygen-level dependent (BOLD) responses in: left SMg extending into and along the length of the intraparietal sulcus (IPS), right IPS, bilateral caudal superior parietal lobule (cSPL), dorsal premotor cortex (dPMC), pre-SMA, and in the lateral cerebellum. Further, region-of-interest analyses revealed interaction effects of fMRI-RS in the experimental versus control condition within left SMg and cerebellum, as well as in bilateral caudal SPL. These efficiency effects cannot be attributed to the repetition of stimulus or response processing, but instead are planning-specific and generally consistent with earlier findings from conventional fMRI investigations. We conclude that repetition-related increases in the efficiency of planning-based selection appears to be associated with parieto-cerebellar networks.

The hand that 'sees' to grasp.

New findings advance our understanding of how vision is used to guide the hand during object grasping.

Human posterior parietal cortex mediates hand-specific planning.

The processes underlying action planning are fundamental to adaptive behavior and can be influenced by recent motor experience. Here, we used a novel fMRI Repetition Suppression (RS) design to test the hypotheses that action planning unfolds more efficiently for successive actions made with the same hand. More efficient processing was predicted to correspond with both faster response times (RTs) to initiate actions and reduced fMRI activity levels - RS. Consistent with these predictions, we detected faster RTs for actions made with the same hand and accompanying fMRI-RS within bilateral posterior parietal cortex and right-lateralized parietal operculum. Within posterior parietal cortex, these RS effects were localized to intraparietal and superior parietal cortices. These same areas were more strongly activated for actions involving the contralateral hand. The findings provide compelling new evidence for the specification of action plans in hand-specific terms, and indicate that these processes are sensitive to recent motor history. Consistent with computational efficiency accounts of motor history effects, the findings are interpreted as evidence for comparatively more efficient processing underlying action planning when successive actions involve the same versus opposite hand.

Two routes to the same action: an action repetition priming study.

Action selection can be influenced by preceding movements. The authors investigated how retrospective factors may interact with plan- versus rule-based action selection. Participants completed 2 tasks, both of which involved selecting a pronated or supinated posture. In the plan task, they chose the most comfortable hand orientation. In the rule task, they followed a learned prescription. Trials in both tasks comprised prime-probe pairs that were identical, or differed in the visual stimulus or required motor response. Both tasks showed a response-time advantage for probes that were preceded by identical primes. This effect was greater for the plan task suggesting that plan-based action selection is especially susceptible to recent history, fortifying the idea that differential mechanisms underlie a rule- versus plan-based approach to the same action.

Hand selection for object grasping is influenced by recent motor history.

Action selection processes such as those that underlie decisions about which hand to use for upcoming actions are fundamental to adaptive motor behavior. Previous research has shown that people grasp objects in ways that reflect anticipated task demands, as well as recent movement experience. However, very few studies have addressed the possible influence of recent motor history on hand selection. In the present study, participants grasped and placed objects using either their left or right hand. The results showed shorter response times to initiate successive actions when hand was repeated, even when those actions involved distinct grasp postures and object placement movements to distinct locations. Conversely, no such planning advantage was observed for repeated grasps for successive actions made with opposite hands. The findings are consistent with the idea that choices about which hand to use in the present are influenced by which hand was used in the recent past. When the same hand can be used for successive actions, planning is made more efficient, presumably because the motor parameters that specify which hand to use can be recalled from recent memory rather than formulated anew. The findings indicate that hand selection is sensitive to recent movement experience and provide novel support for computational efficiency accounts of motor history effects.

Decoding the neural mechanisms of human tool use.

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. DOI:http://dx.doi.org/10.7554/eLife.00425.001.

fMRI repetition suppression for familiar but not arbitrary actions with tools.

For humans, daily life is characterized by routine interaction with many different tools for which corresponding actions are specified and performed according to well-learned procedures. The current study used functional MRI (fMRI) repetition suppression (RS) to identify brain areas underlying the transformation of visually defined tool properties to corresponding motor programs for conventional use. Before grasping and demonstrating how to use a specific tool, participants passively viewed either the same (repeated) tool or a different (non-repeated) tool. Repetition of tools led to reduced fMRI signals (RS) within a selective network of parietal and premotor areas. Comparison with newly learned, arbitrarily defined control actions revealed specificity of RS for tool use, thought to reflect differences in the extent of previous sensorimotor experience. The findings indicate that familiar tools are visually represented within the same sensorimotor areas underlying their dexterous use according to learned properties defined by previous experience. This interpretation resonates with the broader concept of affordance specification considered fundamental to action planning and execution whereby action-relevant object properties (affordances) are visually represented in sensorimotor areas. The current findings extend this view to reveal that affordance specification in humans includes learned object properties defined by previous sensorimotor experience. From an evolutionary perspective, the neural mechanisms identified in the current study offer clear survival advantage, providing fast efficient transformation of visual information to appropriate motor responses based on previous experience.

Decoding action intentions from preparatory brain activity in human parieto-frontal networks.

How and where in the human brain high-level sensorimotor processes such as intentions and decisions are coded remain important yet essentially unanswered questions. This is in part because, to date, decoding intended actions from brain signals has been primarily constrained to invasive neural recordings in nonhuman primates. Here we demonstrate using functional MRI (fMRI) pattern recognition techniques that we can also decode movement intentions from human brain signals, specifically object-directed grasp and reach movements, moments before their initiation. Subjects performed an event-related delayed movement task toward a single centrally located object (consisting of a small cube attached atop a larger cube). For each trial, after visual presentation of the object, one of three hand movements was instructed: grasp the top cube, grasp the bottom cube, or reach to touch the side of the object (without preshaping the hand). We found that, despite an absence of fMRI signal amplitude differences between the planned movements, the spatial activity patterns in multiple parietal and premotor brain areas accurately predicted upcoming grasp and reach movements. Furthermore, the patterns of activity in a subset of these areas additionally predicted which of the two cubes were to be grasped. These findings offer new insights into the detailed movement information contained in human preparatory brain activity and advance our present understanding of sensorimotor planning processes through a unique description of parieto-frontal regions according to the specific types of hand movements they can predict.

To use or to move: goal-set modulates priming when grasping real tools.

How we interact with objects depends on what we intend to do with them. In the current work, we show that priming and the kinematics of grasping depend on the goals of grasping, as well as the context in which tasks are presented. We asked participants to grasp familiar kitchen tools in order to either move them, grasp-to-move (GTM), or to demonstrate their common use, grasp-to-use (GTU). When tasks were blocked separately (Experiment 1), we found that priming was only evident for the GTU task. However, when tasks were presented in the same block of trials (Experiment 2), we observed priming for both tasks. Independent of priming, differences in kinematics and reaction times according to task were evident for both Experiments. Longer reaction times for the GTU task indicate more extensive planning, and differences in grasping reflect the characteristics of subsequent actions. Priming of real grasping is determined by task goals as well as task setting, both of which are likely to modulate how object features (affordances) are perceived and influence the planning of future actions.

Observing learned object-specific functional grasps preferentially activates the ventral stream.

In one popular account of the human visual system, two streams are distinguished, a ventral stream specialized for perception and a dorsal stream specialized for action. The skillful use of familiar tools, however, is likely to involve the cooperation of both streams. Using functional magnetic resonance imaging, we scanned individuals while they viewed short movies of familiar tools being grasped in ways that were either consistent or inconsistent with how tools are typically grasped during use. Typical-for-use actions were predicted to preferentially activate parietal areas important for tool use. Instead, our results revealed several areas within the ventral stream, as well as the left posterior middle temporal gyrus, as preferentially active for our typical-for-use actions. We believe these findings reflect sensitivity to learned semantic associations and suggest a special role for these areas in representing object-specific actions. We hypothesize that during actual tool use a complex interplay between the two streams must take place, with ventral stream areas providing critical input as to how an object should be engaged in accordance with stored semantic knowledge.

fMRI activation during observation of others' reach errors.

When exposed to novel dynamical conditions (e.g., externally imposed forces), neurologically intact subjects easily adjust motor commands on the basis of their own reaching errors. Subjects can also benefit from visual observation of others' kinematic errors. Here, using fMRI, we scanned subjects watching movies depicting another person learning to reach in a novel dynamic environment created by a robotic device. Passive observation of reaching movements (whether or not they were perturbed by the robot) was associated with increased activation in fronto-parietal regions that are normally recruited in active reaching. We found significant clusters in parieto-occipital cortex, intraparietal sulcus, as well as in dorsal premotor cortex. Moreover, it appeared that part of the network that has been shown to be engaged in processing self-generated reach error is also involved in observing reach errors committed by others. Specifically, activity in left intraparietal sulcus and left dorsal premotor cortex, as well as in right cerebellar cortex, was modulated by the amplitude of observed kinematic errors.