High-resolution imaging of skin deformation shows that afferents from human fingertips signal slip onset.

Human tactile afferents provide essential feedback for grasp stability during dexterous object manipulation. Interacting forces between an object and the fingers induce slip events that are thought to provide information about grasp stability. To gain insight into this phenomenon, we made a transparent surface slip against a fixed fingerpad while monitoring skin deformation at the contact. Using microneurography, we simultaneously recorded the activity of single tactile afferents innervating the fingertips. This unique combination allowed us to describe how afferents respond to slip events and to relate their responses to surface deformations taking place inside their receptive fields. We found that all afferents were sensitive to slip events, but fast-adapting type I (FA-I) afferents in particular faithfully encoded compressive strain rates resulting from those slips. Given the high density of FA-I afferents in fingerpads, they are well suited to detect incipient slips and to provide essential information for the control of grip force during manipulation.

Each fingertip hosts thousands of nerve fibers that allow us to handle objects with great dexterity. These fibers relay the amount of friction between the skin and the item, and the brain uses this sensory feedback to adjust the grip as necessary. Yet, exactly how tactile nerve fibers encode information about friction remains largely unknown. Previous research has suggested that friction might not be recorded per se in nerve signals to the brain. Instead, fibers in the finger pad might be responding to localized 'partial slips' that indicate an impending loss of grip. Indeed, when lifting an object, fingertips are loaded with a tangential force that puts strain on the skin, resulting in subtle local deformations. Nerve fibers might be able to detect these skin changes, prompting the brain to adjust an insecure grip before entirely losing grasp of an object. However, technical challenges have made studying the way tactile nerve fibers respond to slippage and skin strain difficult. For the first time, Delhaye et al. have now investigated how these fibers respond to and encode information about the strain placed on fingertips as they are loaded tangentially. A custom-made imaging apparatus was paired with standard electrodes to record the activity of four different kinds of tactile nerve fibers in participants who had a fingertip placed against a plate of glass. The imaging focused on revealing changes in skin surface as tangential force was applied; the electrodes measured impulses from individual nerve fibers from the fingertip. While all the fibers responded during partial slips, fast-adapting type 1 nerves generated strong responses that signal a local loss of grip. Recordings showed that these fibers consistently encoded changes in the skin strain patterns, and were more sensitive to skin compressions related to slippage than to stretch. These results show how tactile nerve fibers encode the subtle skin compressions created when fingers handle objects. The methods developed by Delhaye et al. could further be used to explore the response properties of tactile nerve fibers, sensory feedback and grip.

Grip Stabilization through Independent Finger Tactile Feedback Control.

Grip force control during robotic in-hand manipulation is usually modeled as a monolithic task, where complex controllers consider the placement of all fingers and the contact states between each finger and the gripped object in order to compute the necessary forces to be applied by each finger. Such approaches normally rely on object and contact models and do not generalize well to novel manipulation tasks. Here, we propose a modular grip stabilization method based on a proposition that explains how humans achieve grasp stability. In this biomimetic approach, independent tactile grip stabilization controllers ensure that slip does not occur locally at the engaged robot fingers. Local slip is predicted from the tactile signals of each fingertip sensor i.e., BioTac and BioTac SP by Syntouch. We show that stable grasps emerge without any form of central communication when such independent controllers are engaged in the control of multi-digit robotic hands. The resulting grasps are resistant to external perturbations while ensuring stable grips on a wide variety of objects.

Classification of Transient Myoelectric Signals for the Control of Multi-Grasp Hand Prostheses.

Understanding the neurophysiological signals underlying voluntary motor control and decoding them for controlling limb prostheses is one of the major challenges in applied neuroscience and rehabilitation engineering. While pattern recognition of continuous myoelectric (EMG) signals is arguably the most investigated approach for hand prosthesis control, its underlying assumption is poorly supported, i.e., that repeated muscular contractions produce consistent patterns of steady-state EMGs. In fact, it still remains to be shown that pattern recognition-based controllers allow natural control over multiple grasps in hand prosthesis outside well-controlled laboratory settings. Here, we propose an approach that relies on decoding the intended grasp from forearm EMG recordings associated with the onset of muscle contraction as opposed to the steady-state signals. Eight unimpaired individuals and two hand amputees performed four grasping movements with a variety of arm postures while EMG recordings subsequently processed to mimic signals picked up by conventional myoelectric sensors were obtained from their forearms and residual limbs, respectively. Off-line data analyses demonstrated the feasibility of the approach also with respect to the limb position effect. The sampling frequency and length of the classified EMG window that off-line resulted in optimal performance were applied to a controller of a research prosthesis worn by one hand amputee and proved functional in real-time when operated under realistic working conditions.

Surface strain measurements of fingertip skin under shearing.

The temporal evolution of surface strain, resulting from a combination of normal and tangential loading forces on the fingerpad, was calculated from high-resolution images. A customized robotic device loaded the fingertip with varying normal force, tangential direction and tangential speed. We observed strain waves that propagated from the periphery to the centre of the contact area. Consequently, different regions of the contact area were subject to varying degrees of compression, stretch and shear. The spatial distribution of both the strains and the strain energy densities depended on the stimulus direction. Additionally, the strains varied with the normal force level and were substantial, e.g. peak strains of 50% with a normal force of 5 N, i.e. at force levels well within the range of common dexterous manipulation tasks. While these observations were consistent with some theoretical predictions from contact mechanics, we also observed substantial deviations as expected given the complex geometry and mechanics of fingertips. Specifically, from in-depth analyses, we conclude that some of these deviations depend on local fingerprint patterns. Our data provide useful information for models of tactile afferent responses and background for the design of novel haptic interfaces.

Non-Invasive, Temporally Discrete Feedback of Object Contact and Release Improves Grasp Control of Closed-Loop Myoelectric Transradial Prostheses.

Human grasping and manipulation control critically depends on tactile feedback. Without this feedback, the ability for fine control of a prosthesis is limited in upper limb amputees. Although various approaches have been investigated in the past, at present there is no commercially available device able to restore tactile feedback in upper limb amputees. Based on the Discrete Event-driven Sensory feedback Control (DESC) policy we present a device able to deliver short-lasting vibrotactile feedback to transradial amputees using commercially available myoelectric hands. The device (DESC-glove) comprises sensorized thimbles to be placed on the prosthesis digits, a battery-powered electronic board, and vibrating units embedded in an arm-cuff being transiently activated when the prosthesis makes and breaks contact with objects. The consequences of using the DESC-glove were evaluated in a longitudinal study. Five transradial amputees were equipped with the device for one month at home. Through a simple test proposed here for the first time-the virtual eggs test-we demonstrate the effectiveness of the device for prosthetic control in daily life conditions. In the future the device could be easily exploited as an add-on to complement myoelectric prostheses or even embedded in prosthetic sockets to enhance their control by upper limb amputees.

Humans can integrate feedback of discrete events in their sensorimotor control of a robotic hand.

Providing functionally effective sensory feedback to users of prosthetics is a largely unsolved challenge. Traditional solutions require high band-widths for providing feedback for the control of manipulation and yet have been largely unsuccessful. In this study, we have explored a strategy that relies on temporally discrete sensory feedback that is technically simple to provide. According to the Discrete Event-driven Sensory feedback Control (DESC) policy, motor tasks in humans are organized in phases delimited by means of sensory encoded discrete mechanical events. To explore the applicability of DESC for control, we designed a paradigm in which healthy humans operated an artificial robot hand to lift and replace an instrumented object, a task that can readily be learned and mastered under visual control. Assuming that the central nervous system of humans naturally organizes motor tasks based on a strategy akin to DESC, we delivered short-lasting vibrotactile feedback related to events that are known to forcefully affect progression of the grasp-lift-and-hold task. After training, we determined whether the artificial feedback had been integrated with the sensorimotor control by introducing short delays and we indeed observed that the participants significantly delayed subsequent phases of the task. This study thus gives support to the DESC policy hypothesis. Moreover, it demonstrates that humans can integrate temporally discrete sensory feedback while controlling an artificial hand and invites further studies in which inexpensive, noninvasive technology could be used in clever ways to provide physiologically appropriate sensory feedback in upper limb prosthetics with much lower band-width requirements than with traditional solutions.

Biting intentions modulate digastric reflex responses to sudden unloading of the jaw.

Reflex responses in jaw-opening muscles can be evoked when a brittle object cracks between the teeth and suddenly unloads the jaw. We hypothesized that this reflex response is flexible and, as such, is modulated according to the instructed goal of biting through an object. Study participants performed two different biting tasks when holding a peanut half stacked on a chocolate piece between their incisors. In one task, they were asked to split the peanut half only (single-split task), and in the other task, they were asked to split both the peanut and the chocolate in one action (double-split task). In both tasks, the peanut split evoked a jaw-opening muscle response, quantified from electromyogram (EMG) recordings of the digastric muscle in a window 20-60 ms following peanut split. Consistent with our hypothesis, we found that the jaw-opening muscle response in the single-split trials was about twice the size of the jaw-opening muscle response in the double-split trials. A linear model that predicted the jaw-opening muscle response on a single-trial basis indicated that task settings played a significant role in this modulation but also that the presplit digastric muscle activity contributed to the modulation. These findings demonstrate that, like reflex responses to mechanical perturbations in limb muscles, reflex responses in jaw muscles not only show gain-scaling but also are modulated by subject intent.

Task-dependent control of the jaw during food splitting in humans.

Although splitting of food items between the incisors often requires high bite forces, rarely do the teeth harmfully collide when the jaw quickly closes after split. Previous studies indicate that the force-velocity relationship of the jaw closing muscles principally explains the prompt dissipation of jaw closing force. Here, we asked whether people could regulate the dissipation of jaw closing force during food splitting. We hypothesized that such regulation might be implemented via differential recruitment of masseter muscle portions situated along the anteroposterior axis because these portions will experience a different shortening velocity during jaw closure. Study participants performed two different tasks when holding a peanut-half stacked on a chocolate piece between their incisors. In one task, they were asked to split the peanut-half only (single-split trials) and, in the other, to split both the peanut and the chocolate in one action (double-split trials). In double-split trials following the peanut split, the intensity of the tooth impact on the chocolate piece was on average 2.5 times greater than in single-split trials, indicating a substantially greater loss of jaw closing force in the single-split trials. We conclude that control of jaw closing force dissipation following food splitting depends on task demands. Consistent with our hypothesis, converging neurophysiological and morphometric data indicated that this control involved a differential activation of the jaw closing masseter muscle along the anteroposterior axis. These latter findings suggest that the regulation of jaw closing force after sudden unloading of the jaw exploits masseter muscle compartmentalization.

Multi-channel EEG recordings during 3,936 grasp and lift trials with varying weight and friction.

WAY-EEG-GAL is a dataset designed to allow critical tests of techniques to decode sensation, intention, and action from scalp EEG recordings in humans who perform a grasp-and-lift task. Twelve participants performed lifting series in which the object's weight (165, 330, or 660 g), surface friction (sandpaper, suede, or silk surface), or both, were changed unpredictably between trials, thus enforcing changes in fingertip force coordination. In each of a total of 3,936 trials, the participant was cued to reach for the object, grasp it with the thumb and index finger, lift it and hold it for a couple of seconds, put it back on the support surface, release it, and, lastly, to return the hand to a designated rest position. We recorded EEG (32 channels), EMG (five arm and hand muscles), the 3D position of both the hand and object, and force/torque at both contact plates. For each trial we provide 16 event times (e.g., 'object lift-off') and 18 measures that characterize the behaviour (e.g., 'peak grip force').

Cognitive function and other risk factors for mild traumatic brain injury in young men: nationwide cohort study.

OBJECTIVE: To investigate cognitive function and other risk factors for mild traumatic brain injury in young men. DESIGN: Nationwide prospective cohort study. SETTING: Sweden. PARTICIPANTS: 305 885 men conscripted for military service from 1989 to 1994. MAIN OUTCOME MEASURE: mild traumatic brain injuries in relation to cognitive function and other potential risk factors assessed at conscription and follow-up. RESULTS: Men with one mild traumatic brain injury within two years before (n=1988) or after cognitive testing (n=2214) had about 5.5% lower overall cognitive function scores than did men with no mild traumatic brain injury during follow up (P<0.001 for both). Moreover, men with at least two mild traumatic brain injuries after cognitive testing (n=795) had 15% lower overall cognitive function scores compared with those with no such injury (P<0.001). Independent strong risk factors (P<1×10(-10)) for at least one mild traumatic brain injury after cognitive testing (n=12 494 events) included low overall cognitive function, a previous mild traumatic brain injury, hospital admission for intoxications, and low education and socioeconomic status. In a sub-cohort of twin pairs in which one twin had a mild traumatic brain injury before cognitive testing (n=63), both twins had lower logical performance and technical performance compared with men in the total cohort with no mild traumatic brain injury (P<0.05 for all). CONCLUSION: Low cognitive function, intoxications, and factors related to low socioeconomic status were strong independent risk factors for mild traumatic brain injuries in men. The low cognitive function in twin pairs discordant for mild traumatic brain injury suggests a genetic component to the low cognitive function associated with such injuries. The study included only men, so inferences to women should be made with caution.

A modified low-cost haptic interface as a tool for complex tactile stimulation.

This study describes the development and evaluation of a platform for the investigation of the human tactile ability. Specifically, it enables precise and reproducible application of time-varying 3D force stimuli to the skin of an immobilized human limb. We proceeded in the following steps: (1) programming a low-cost haptic interface to apply time-varying 3D force stimuli to a fixed rigid target, (2) implementing a combined feed-forward/feedback controller to improve the platform's precision and reliability in force stimulation, (3) determining the optimal tuning of the control loop parameters and (4) evaluating the system's performances when applying time-varying 3D force stimuli to an immobilized human finger pad. The system's performances were evaluated in terms of the accuracy and repeatability when delivering standard 3D force stimuli, i.e., stimuli with specified force components in the normal and skin tangential directions. Within the range of forces tested (5 N in various directions), the maximum difference between the actual force and the desired value during static phases was <30 mN (accuracy) and the root-mean-square of the standard deviation (repeatability) was 15 mN during static phases and <75 mN during dynamic phases.

Human ability to discriminate direction of three-dimensional force stimuli applied to the finger pad.

Sensory information from tactile mechanoreceptors located in the glabrous skin of the hand is crucial for skillful object exploration and manipulation. These mechanoreceptors reliably encode the direction of fingertip forces, and the brain certainly relies on this information in both sensorimotor and cognitive tasks. In this study, we examined human ability to discriminate the direction of force stimuli applied to the volar surface of the index fingertip on the basis of tactile information only. We show that humans can discriminate three-dimensional (3D) force stimuli whose directions differ by an angle as small as 7.1 ° in the plane tangential to the skin surface. Moreover, we found that the discrimination ability was mainly affected by the time-varying phases of the stimulus, because adding a static plateau phase to the stimulus improved the discrimination threshold only to a limited extent.

Human muscle spindles act as forward sensory models.

Modern theories of motor control incorporate forward models that combine sensory information and motor commands to predict future sensory states. Such models circumvent unavoidable neural delays associated with on-line feedback control. Here we show that signals in human muscle spindle afferents during unconstrained wrist and finger movements predict future kinematic states of their parent muscle. Specifically, we show that the discharges of type Ia afferents are best correlated with the velocity of length changes in their parent muscles approximately 100-160 ms in the future and that their discharges vary depending on motor sequences in a way that cannot be explained by the state of their parent muscle alone. We therefore conclude that muscle spindles can act as "forward sensory models": they are affected both by the current state of their parent muscle and by efferent (fusimotor) control, and their discharges represent future kinematic states. If this conjecture is correct, then sensorimotor learning implies learning how to control not only the skeletal muscles but also the fusimotor system.

Humans can integrate force feedback to toes in their sensorimotor control of a robotic hand.

Tactile sensory feedback is essential for dexterous object manipulation. Users of hand myoelectric prostheses without tactile feedback must depend essentially on vision to control their device. Indeed, improved tactile feedback is one of their main priorities. Previous research has provided evidence that conveying tactile feedback can improve prostheses control, although additional effort is required to solve problems related to pattern recognition learning, unpleasant sensations, sensory adaptation, and low spatiotemporal resolution. Still, these studies have mainly focused on providing stimulation to hairy skin regions close to the amputation site, i.e., usually to the upper arm. Here, we explored the possibility to provide tactile feedback to the glabrous skin of toes, which have mechanical and neurophysiological properties similar to the fingertips. We explored this paradigm in a grasp-and-lift task, in which healthy participants controlled two opposing digits of a robotic hand by changing the spacing of their index finger and thumb. The normal forces applied by the robotic fingertips to a test object were fed back to the right big and second toe. We show that within a few lifting trials, all the participants incorporated the force feedback received by the foot in their sensorimotor control of the robotic hand.

Discharges in human muscle receptor afferents during block grasping.

Human grasping relies on feedforward control that is monitored and corrected on-line by means of sensory feedback. While much of the sensory mechanisms underpinning hand-object interaction are known, information has been lacking about muscle receptor responses during the phases before and after actual object contact. We therefore let subjects use their thumb and fingers to grasp blocks presented to them while we recorded muscle afferents from the thumb and finger extensor muscles along with wrist and digit kinematics, and electromyographic activity. The kinematics of the task was indistinguishable from "normal" grasping. None of the afferents encoded either object contact or finger apposition. Both primary and secondary afferents were more phase advanced on the parent muscle lengths than expected from previous studies as well as from their responses to imposed length changes of their parent muscles. Thus, the discharges of both primary and secondary afferents were well correlated to the tendon velocity of their parent muscles and that of primary afferents also to acceleration whereas neither appeared to encode muscle length as such. Decoding the velocity of muscle length changes were significantly improved if the discharge of Golgi tendon organ afferents were taken into account along with that of the muscle spindle afferents. We propose that these findings may be explained by the biomechanical properties of contracting muscles. Moreover, we conclude that it seems unlikely that the muscle spindle afferents recorded in this task have any role in providing "proprioceptive" information pertaining to the size of an object grasped.

Discharges in human muscle spindle afferents during a key-pressing task.

Most manual tasks demand a delicate control of the wrist. Sensory information for this control, e.g. about the position and movement velocity of the hand, is assumed to be primarily provided by muscle spindle afferents. It is known that human muscle spindles in relaxed muscles behave as stretch receptors but it is unclear how they discharge during 'natural' hand movements, since their discharges can also be affected by extrafusal contractions and fusimotor activity. We therefore let subjects perform a centre-out-centre key-pressing task on buttons laid out in a 3 x 3 pattern, a task that allowed unconstrained hand and finger movements and required precise control of the wrist. Microneurography recordings from muscle spindle afferents of the wrist extensor muscles were obtained along with wrist kinematics and electromyographic signals. The discharge rates of afferents were more phase advanced than expected on the length of the radial wrist extensor, which acted as an anti-gravity muscle in the key-pressing task. As such, both acceleration and velocity had significant impacts on the discharge rate of primary afferents, velocity on that of secondary afferents, and length had no impact on either afferent type. The response patterns were different for the two types of muscle spindle afferents from the predominantly eccentrically contracting ulnar wrist extensor: muscle length and velocity had significant impacts on the ensemble response of secondary afferents whereas the primary afferents showed highly variable responses. Accordingly, good predictions of the radial ulnar angular velocity were possible from spindle ensemble responses (R(2) = 0.85) whereas length could be predicted only for phases with lengthening of the ulnar wrist extensor. There are several possible explanations for the unexpectedly large phase advance of spindle afferents in the radial wrist extensor. Given the compliance of tendons, for instance, the phase relationship between the muscle fascicle length and the whole muscle length is conjectured to depend on the load. While additional phase advances are advantageous in motor control, it is concluded that if the central nervous system estimates length or velocity of a muscle from its muscle spindle discharges, this would require additional information about not only the concomitant extrafusal and fusimotor drive but also about the mechanical properties of the load on which the muscle acts.

Prediction of object contact during grasping.

The maximum grip aperture (MGA) during prehension is linearly related to the size of objects to be grasped and is adapted to the haptically sensed object size when there is a discrepancy between visual and haptic information. We have investigated what information is used to drive this adaptation process and how the onset of fingertip forces on the object is triggered. Subjects performed a reach-to-grasp task, where the object seen and the object grasped physically never were the same. We measured the movements of the index finger and the thumb and the contact forces between each fingertip and the object. The subjects' adaptation of the MGA was unrelated both to different fingertip velocities at the moment of object contact, or the fingertip forces. Instead, the 'timing' of contact between the fingers and the object was most consistently influenced by introducing a size discrepancy. Specifically, if the object was larger than expected, the moment of contact occurred earlier, and if the object was decreased in size, then the contact occurred later. During adaptation, these timing differences were markedly reduced. Also, the motor command for applying forces on the object seemed to be released in anticipation of the predicted moment of contact. We therefore conclude that the CNS dynamically predicts when contact between the fingertips and objects occur and that aperture adaptation is primarily driven by timing prediction errors.

Acquiring and adapting a novel audiomotor map in human grasping.

For sensorimotor transformations to be executed accurately, there must be mechanisms that can both establish and modify mappings between sensory and motor coordinates. Such mechanisms were investigated in normal subjects using a reach-to-grasp task. First, we replaced the normal input of visual information about object size with auditory information, i.e., we attempted to establish an 'audiomotor map'. The size of the object was log linearly related to the frequency of the sound, and we measured the maximum grip aperture (MGA) during the reaching phase to determine if the subjects had learned the relationship. Second, we changed the frequency-object size relationship to study adaptation in the newly acquired map. Our results demonstrate that learning of an audiomotor map consisted of three distinct phases: during the first stage (approximately 10-15 trials) subjects simply used MGAs large enough to grasp any reasonably sized object and there were no overt signs of learning. During the second stage, there was a period of fast learning where the slope of the relationship between MGA and object size became steeper until the third stage where the slope was constant. In contrast, when sensorimotor adaptation was studied in the established audiomotor map, there was rapid learning from the start of a size perturbation. We conclude that different learning strategies are employed when sensorimotor transformations are established compared to when existing transformations are modified.

Short-term plasticity of the visuomotor map during grasping movements in humans.

During visually guided grasping movements, visual information is transformed into motor commands. This transformation is known as the "visuomotor map." To investigate limitations in the short-term plasticity of the visuomotor map in normal humans, we studied the maximum grip aperture (MGA) during the reaching phase while subjects grasped objects of various sizes. The objects seen and the objects grasped were physically never the same. When a discrepancy had been introduced between the size of the visual and the grasped objects, and the subjects were fully adapted to it, they all readily interpolated and extrapolated the MGA to objects not included in training trials. In contrast, when the subjects were exposed to discrepancies that required a slope change in the visuomotor map, they were unable to adapt adequately. They instead retained a subject-specific slope of the relationship between the visual size and MGA. We conclude from these results that during reaching for grasping, normal subjects are unable to abandon a straight linear function determining the relationship between visual object size and MGA. Moreover, the plasticity of the visuomotor map is, at least in short term, constrained to allow only offset changes, that is, only "rigid shifts" are possible between the visual and motor coordinate systems.