Skin properties and afferent density in the deterioration of tactile spatial acuity with age.

Tactile sensitivity is affected by age, as shown by the deterioration of spatial acuity assessed with the two-point discrimination task. This is assumed to be partly a result of age-related changes of the peripheral somatosensory system. In particular, in the elderly, the density of mechanoreceptive afferents decreases with age and the skin tends to become drier, less elastic and less stiff. To assess to what degree mechanoreceptor density, skin hydration, elasticity and stiffness can account for the deterioration of tactile spatial sensitivity observed in the elderly, several approaches were combined, including psychophysics, measurements of finger properties, modelling and simulation of the response of first-order tactile neurons. Psychophysics confirmed that the Elderly group has lower tactile acuity than the Young group. Correlation and commonality analysis showed that age was the most important factor in explaining decreases in behavioural performance. Biological elasticity, hydration and finger pad area were also involved. These results were consistent with the outcome of simulations showing that lower afferent density and lower Young's modulus (i.e. lower stiffness) negatively affected the tactile encoding of stimulus information. Simulations revealed that these changes resulted in a lower build-up of task-relevant stimulus information. Importantly, the reduction in discrimination performance with age in the simulation was less than that observed in the psychophysical testing, indicating that there are additional peripheral as well as central factors responsible for age-related changes in tactile discrimination. KEY POINTS: Ageing effects on tactile perception involve the deterioration of spatial sensitivity, although the contribution of central and peripheral factors is not clear. We combined psychophysics, measurements of finger properties, modelling and simulation of the response of first-order tactile neurons to investigate to what extent skin elasticity, stiffness, hydration, finger pad area and afferent density can account for the lower spatial sensitivity observed in the elderly. Correlation and commonality analysis revealed that age was the most important factor to predict behavioural performance. Skin biological elasticity, hydration and finger pad area contributed to a lesser extent. The simulation of first-order tactile neuron responses indicated that reduction in afferent density plays a major role in the deterioration of tactile spatial acuity. Simulations also showed that lower skin stiffness and lower afferent density affect the build-up of stimulus information and the response of SA1 (i.e. type 1 slowly adapting fibres) and RA1 (i.e. type 1 rapidly adapting fibres) afferent fibres.

Boosting robot-assisted rehabilitation of stroke hemiparesis by individualized selection of upper limb movements - a pilot study.

BACKGROUND: Intensive robot-assisted training of the upper limb after stroke can reduce motor impairment, even at the chronic stage. However, the effectiveness of practice for recovery depends on the selection of the practised movements. We hypothesized that rehabilitation can be optimized by selecting the movements to be practiced based on the trainee's performance profile. METHODS: We present a novel principle ('steepest gradients') for performance-based selection of movements. The principle is based on mapping motor performance across a workspace and then selecting movements located at regions of the steepest transition between better and worse performance. To assess the benefit of this principle we compared the effect of 15 sessions of robot-assisted reaching training on upper-limb motor impairment, between two groups of people who have moderate-to-severe chronic upper-limb hemiparesis due to stroke. The test group (N = 7) received steepest gradients-based training, iteratively selected according to the steepest gradients principle with weekly remapping, whereas the control group (N = 9) received a standard "centre-out" reaching training. Training intensity was identical. RESULTS: Both groups showed improvement in Fugl-Meyer upper-extremity scores (the primary outcome measure). Moreover, the test group showed significantly greater improvement (twofold) compared to control. The score remained elevated, on average, for at least 4 weeks although the additional benefit of the steepest-gradients -based training diminished relative to control. CONCLUSIONS: This study provides a proof of concept for the superior benefit of performance-based selection of practiced movements in reducing upper-limb motor impairment due to stroke. This added benefit was most evident in the short term, suggesting that performance-based steepest-gradients training may be effective in increasing the rate of initial phase of practice-based recovery; we discuss how long-term retention may also be improved. TRIAL REGISTRATION: ISRCTN, ISRCTN65226825 , registered 12 June 2018 - Retrospectively registered.

Correction to: Boosting robot-assisted rehabilitation of stroke hemiparesis by individualized selection of upper limb movements - a pilot study.

The original article [1] contained a minor error in the following sentence in the Discussion.

Stepping to an Auditory Metronome Improves Weight-Bearing Symmetry in Poststroke Hemiparesis.

Asymmetry in weight-bearing is a common feature in poststroke hemiparesis and is related to temporal asymmetry during walking. The aim of this study was to investigate the effect of an auditory cue for stepping in place on measures of temporal and weight-bearing asymmetry. A total of 10 community-dwelling adults (6 males and 4 females) with chronic poststroke hemiparesis performed 5 un-cued stepping trials and 5 stepping trials cued by an auditory metronome cue. A Vicon system was used to collect full body kinematic trajectories. Two force platforms were used to measure ground reaction forces. Step, swing, and stance times were used to calculate temporal symmetry ratios. Weight-bearing was assessed using the vertical component of the ground reaction force and center of mass-center of pressure separation at mid-stance. Weight-bearing asymmetry was significantly reduced during stepping with an auditory cue. Asymmetry values for step, swing, and stance times were also significantly reduced with auditory cueing. These findings show that auditory cueing when stepping in place produces immediate reductions in measures of temporal asymmetry and dynamic weight-bearing asymmetry.

Afferent motor feedback determines the perceived location of tactile stimuli in the external space presented to the moving arm.

People make systematic errors when localizing a brief tactile stimulus in the external space presented on the index finger while moving the arm. Although these errors likely arise in the spatiotemporal integration of the tactile input and information about arm position, the underlying arm position information used in this process is not known. In this study, we tested the contributions of afferent proprioceptive feedback and predictive arm position signals by comparing localization errors during passive vs. active arm movements. In the active trials, participants were instructed to localize a tactile stimulus in the external space that was presented to the index finger near the time of a self-generated arm movement. In the passive trials, each of the active trials was passively replayed in randomized order, using a robotic device. Our results provide evidence that the localization error patterns of the passive trials are similar to the active trials and, moreover, did not lag but rather led the active trials, which suggests that proprioceptive feedback makes an important contribution to tactile localization. To further test which kinematic property of this afferent feedback signal drives the underlying computations, we examined the localization errors with movements that had differently skewed velocity profiles but overall the same displacement. This revealed a difference in the localization patterns, which we explain by a probabilistic model in which temporal uncertainty about the stimulus is converted into a spatial likelihood, depending on the actual velocity of the arm rather than involving an efferent, preprogrammed movement.NEW & NOTEWORTHY We show that proprioceptive feedback of arm motion rather than efferent motor signals contributes to tactile localization during an arm movement. Data further show that localization errors depend on arm velocity, not displacement per se, suggesting that instantaneous velocity feedback plays a role in the underlying computations. Model simulation using Bayesian inference suggests that these errors depend not only on spatial but also on temporal uncertainties of sensory and motor signals.

Mapping upper-limb motor performance after stroke - a novel method with utility for individualized motor training.

BACKGROUND: Chronic upper limb motor impairment is a common outcome of stroke. Therapeutic training can reduce motor impairment. Recently, a growing interest in evaluating motor training provided by robotic assistive devices has emerged. Robot-assisted therapy is attractive because it provides a means of increasing practice intensity without increasing the workload of physical therapists. However, movements practised through robotic assistive devices are commonly pre-defined and fixed across individuals. More optimal training may result from individualizing the selection of the trained movements based on the individual's impairment profile. This requires quantitative assessment of the degree of the motor impairment prior to training, in relevant movement tasks. However, standard clinical measures for profiling motor impairment after stroke are often subjective and lack precision. We have developed a novel robot-mediated method for systematic and fine-grained mapping (or profiling) of individual performance across a wide range of planar arm reaching movements. Here we describe and demonstrate this mapping method and its utilization for individualized training. We also present a novel principle for the individualized selection of training movements based on the performance maps. METHODS AND RESULTS: To demonstrate the utility of our method we present examples of 2D performance maps produced from the kinetic and kinematics data of two individuals with stroke-related upper limb hemiparesis. The maps outline distinct regions of high motor impairment. The procedure of map-based selection of training movements and the change in motor performance following training is demonstrated for one participant. CONCLUSIONS: The performance mapping method is feasible to produce (online or offline). The 2D maps are easy to interpret and to be utilized for selecting individual performance-based training. Different performance maps can be easily compared within and between individuals, which potentially has diagnostic utility.

Selecting object pairs for action: Is the active object always first?

Perception is linked to action via two routes: a direct route based on affordance information in the environment and an indirect route based on semantic knowledge about objects. The present study explored the factors modulating the recruitment of the two routes, in particular which factors affecting the selection of paired objects. In Experiment 1, we presented real objects among semantically related or unrelated distracters. Participants had to select two objects that can interact. The presence of distracters affected selection times, but not the semantic relations of the objects with the distracters. Furthermore, participants first selected the active object (e.g. teaspoon) with their right hand, followed by the passive object (e.g. mug), often with their left hand. In Experiment 2, we presented pictures of the same objects with no hand grip, congruent or incongruent hand grip. Participants had to decide whether the two objects can interact. Action decisions were faster when the presentation of the active object preceded the presentation of the passive object, and when the grip was congruent. Interestingly, participants were slower when the objects were semantically but not functionally related; this effect increased with congruently gripped objects. Our data showed that action decisions in the presence of strong affordance cues (real objects, pictures of congruently gripped objects) relied on sensory-motor representation, supporting the direct route from perception-to-action that bypasses semantic knowledge. However, in the case of weak affordance cues (pictures), semantic information interfered with action decisions, indicating that semantic knowledge impacts action decisions. The data support the dual-route account from perception-to-action.

Contribution of the motor system to the perception of reachable space: an fMRI study.

The present functional magnetic resonance imaging (fMRI) study investigates the neural correlates of reachability judgements. In a block design experiment, 14 healthy participants judged whether a visual target presented at different distances in a virtual environment display was reachable or not with the right hand. In two control tasks, they judged the colour or the relative position of the visual target according to flankers. Contrasting the activations registered in the reachability judgement task and in the control tasks, we found activations in the frontal structures, and in the bilateral inferior and superior parietal lobe, including the precuneus, and the bilateral cerebellum. This fronto-parietal network including the cerebellum overlaps with the brain network usually activated during actual motor production and motor imagery. In a following event-related design experiment, we contrasted brain activations when targets were rated as 'reachable' with those when they were rated as 'unreachable'. We found activations in the left premotor cortex, the bilateral frontal structures, and the left middle temporal gyrus. At a lower threshold, we also found activations in the left motor cortex, and in the bilateral cerebellum. Given that reaction time increased with target distance in reachable space, we performed a subsequent parametric analysis that revealed a related increase of activity in the fronto-parietal network including the cerebellum. Unreachable targets did not show similar activation, and particularly in regions associated to motor production and motor imagery. Taken together, these results suggest that dynamical motor representations used to determine what is reachable are also part of the perceptual process leading to the distinct representation of peripersonal and extrapersonal spaces.

Moving in time: Bayesian causal inference explains movement coordination to auditory beats.

Many everyday skilled actions depend on moving in time with signals that are embedded in complex auditory streams (e.g. musical performance, dancing or simply holding a conversation). Such behaviour is apparently effortless; however, it is not known how humans combine auditory signals to support movement production and coordination. Here, we test how participants synchronize their movements when there are potentially conflicting auditory targets to guide their actions. Participants tapped their fingers in time with two simultaneously presented metronomes of equal tempo, but differing in phase and temporal regularity. Synchronization therefore depended on integrating the two timing cues into a single-event estimate or treating the cues as independent and thereby selecting one signal over the other. We show that a Bayesian inference process explains the situations in which participants choose to integrate or separate signals, and predicts motor timing errors. Simulations of this causal inference process demonstrate that this model provides a better description of the data than other plausible models. Our findings suggest that humans exploit a Bayesian inference process to control movement timing in situations where the origin of auditory signals needs to be resolved.

Preliminary evaluation of a personal healthcare system prototype for cognitive eRehabilitation in a living assistance domain.

The integration of rehabilitation systems in an ambient assisted living environment can provide a powerful and versatile tool for long-term stroke rehabilitation goals. This paper introduces a novel concept of a personalized cognitive rehabilitation system in a naturalistic setting. The proposed platform was developed within the CogWatch project, with the intent of fostering independence in activities of daily living in patients with apraxia and action disorganization syndrome. Technical usability was evaluated in a series of pilot experiments, which illustrate how this approach may help to retrain patients in activities of daily living. The first system prototype has been tested with 36 participants divided into three groups, providing an exploratory evaluation of the usability of this solution and its acceptability. The technical solutions used within the CogWatch project are targeted to meet both the end users' needs from the interaction and usability point of views and the clinical requirements associated with the use of such systems. The challenges behind the development of ambient assisted living systems for cognitive rehabilitation are discussed.

Spatiotemporal integration for tactile localization during arm movements: a probabilistic approach.

It has been shown that people make systematic errors in the localization of a brief tactile stimulus that is delivered to the index finger while they are making an arm movement. Here we modeled these spatial errors with a probabilistic approach, assuming that they follow from temporal uncertainty about the occurrence of the stimulus. In the model, this temporal uncertainty converts into a spatial likelihood about the external stimulus location, depending on arm velocity. We tested the prediction of the model that the localization errors depend on arm velocity. Participants (n = 8) were instructed to localize a tactile stimulus that was presented to their index finger while they were making either slow- or fast-targeted arm movements. Our results confirm the model's prediction that participants make larger localization errors when making faster arm movements. The model, which was used to fit the errors for both slow and fast arm movements simultaneously, accounted very well for all the characteristics of these data with temporal uncertainty in stimulus processing as the only free parameter. We conclude that spatial errors in dynamic tactile perception stem from the temporal precision with which tactile inputs are processed.

Evidence for vibration coding of sliding tactile textures in auditory cortex.

Introduction: Psychophysical studies suggest texture perception is mediated by spatial and vibration codes (duplex theory). Vibration coding, driven by relative motion between digit and stimulus, is involved in the perception of very fine gratings whereas coarse texture perception depends more on spatial coding, which does not require relative motion. Methods: We examined cortical activation, using functional Magnetic Resonance Imaging associated with fine and coarse tactile spatial gratings applied by sliding or touching (sliding vs. static contact) on the index finger pad. Results: We found regions, contralateral to the stimulated digit, in BA1 in S1, OP1, OP3, and OP4 in S2, and in auditory cortex, which were significantly more activated by sliding gratings but did not find this pattern in visual cortex. Regions in brain areas activated by vibrotactile stimuli (including auditory cortex) were also modulated by whether or not the gratings moved. In a control study we showed that this contrast persisted when the salience of the static condition was increased by using a double touch. Discussion: These findings suggest that vibration from sliding touch invokes multisensory cortical mechanisms in tactile processing of roughness. However, we did not find evidence of a separate visual region activated by static touch nor was there a dissociation between cortical response to fine vs. coarse gratings as might have been expected from duplex theory.

Contrasting effects of finger and shoulder interpersonal light touch on standing balance.

Sway is reduced by light nonsupporting touch between parts of the body and a fixed surface. This effect is assumed to reflect augmentation of sensory cues for sway by point-of-contact reaction forces. It has been shown that movement of the contact surface can increase sway relative to an earth-fixed contact. Light touch contact with another person, for example, holding hands, affords a moving contact due to partner sway. We asked whether interpersonal light touch (IPLT) would increase sway relative to standing alone. We expected effects on sway to vary as a function of the site of contact and the postural stability of each partner. Eight pairs of participants, standing in either normal bipedal or tandem Romberg stance with eyes closed and using IPLT (finger to finger or shoulder to shoulder) or no contact, provided 4 trials of 30-s duration in each of 12 posture-touch combinations. Sway (SD of the rate of change of upper trunk position at C7) was reliably less with IPLT compared with no contact, with two exceptions: in normal stance, shoulder contact with a partner in tandem stance, and in tandem Romberg stance, finger contact with a partner in the same stance, increased sway. Otherwise, the reduction in sway was greater with shoulder than with finger contact. Measures of interpersonal synchronization based on cross-correlations and coherence analysis between the partners' C7 movements suggest different control factors operate to reduce sway in IPLT with the hand or shoulder contact.

Impaired predictive timing with spared time interval production in individual with schizophrenia.

There is evidence for timing dysfunctions in schizophrenia. However, few studies have evaluated the processing of intervals in the hundreds of milliseconds range, despite their role in the timing of speech, music and movements. This study looked into the prediction and estimation mechanisms for intervals in that time range in individuals with schizophrenia and age-matched neurotypical controls. Specifically, we questioned the capacity of the patients to detect a phase shift that requires the processing of a deviation from 'what should happen when' given prior event regularity. The minimum detectable phase shift was estimated from an adaptive staircase procedure with or without the need for sensorimotor synchronization. Results revealed that patients were significantly impaired relative to controls, at each of the tested inter-onset intervals (IOI=300, 600 and 900ms). A control experiment used the method of repeated interval production to show that both groups performed similarly in the production of target intervals (T=500ms and 1000ms). We conclude that schizophrenia is associated with predictive timing deficits, which cannot be attributed directly to a faster or slower running internal clock.

Skin and Mechanoreceptor Contribution to Tactile Input for Perception: A Review of Simulation Models.

We review four current computational models that simulate the response of mechanoreceptors in the glabrous skin to tactile stimulation. The aim is to inform researchers in psychology, sensorimotor science and robotics who may want to implement this type of quantitative model in their research. This approach proves relevant to understanding of the interaction between skin response and neural activity as it avoids some of the limitations of traditional measurement methods of tribology, for the skin, and neurophysiology, for tactile neurons. The main advantage is to afford new ways of looking at the combined effects of skin properties on the activity of a population of tactile neurons, and to examine different forms of coding by tactile neurons. Here, we provide an overview of selected models from stimulus application to neuronal spiking response, including their evaluation in terms of existing data, and their applicability in relation to human tactile perception.

The efficacy of a task model approach to ADL rehabilitation in stroke apraxia and action disorganisation syndrome: A randomised controlled trial.

BACKGROUND: Apraxia and action disorganization syndrome (AADS) after stroke can disrupt activities of daily living (ADL). Occupational therapy has been effective in improving ADL performance, however, inclusion of multiple tasks means it is unclear which therapy elements contribute to improvement. We evaluated the efficacy of a task model approach to ADL rehabilitation, comparing training in making a cup of tea with a stepping training control condition. METHODS: Of the 29 stroke survivors with AADS who participated in this cross-over randomized controlled feasibility trial, 25 were included in analysis [44% females; mean(SD) age = 71.1(7.8) years; years post-stroke = 4.6(3.3)]. Participants attended five 1-hour weekly tea making training sessions in which progress was monitored and feedback given using a computer-based system which implemented a Markov Decision Process (MDP) task model. In a control condition, participants received five 1-hour weekly stepping sessions. RESULTS: Compared to stepping training, tea making training reduced errors across 4 different tea types. The time taken to make a cup of tea was reduced so the improvement in accuracy was not due to a speed-accuracy trade-off. No improvement linked to tea making training was evident in a complex tea preparation task (making two different cups of tea simultaneously), indicating a lack of generalisation in the training. CONCLUSIONS: The clearly specified but flexible training protocol, together with information on the distribution of errors, provide pointers for further refinement of task model approaches to ADL rehabilitation. It is recommended that the approach be tested under errorless learning conditions with more impaired patients in future research. TRIAL REGISTRATION: Retrospectively registered at ClinicalTrials.gov on 5th August 2019 [NCT04044911] https://clinicaltrials.gov/ct2/show/NCT04044911?term=Cogwatch&rank=1.

The effect of ageing on multisensory integration for the control of movement timing.

Previously, it has been shown that synchronising actions with periodic pacing stimuli are unaffected by ageing. However, synchronisation often requires combining evidence across multiple sources of timing information. We have previously shown the brain integrates multisensory cues to achieve a best estimate of the events in time and subsequently reduces variability in synchronised movements (Elliott et al. in Eur J Neurosci 31(10):1828-1835, 2010). Yet, it is unclear if sensory integration of temporal cues in older adults is degraded and whether this leads to reduced synchronisation performance. Here, we test for age-related changes when synchronising actions to multisensory temporal cues. We compared synchronisation performance between young (N = 15, aged 18-37 years) and older adults (N = 15, aged 63-80 years) using a finger-tapping task to auditory and tactile metronomes presented unimodally and bimodally. We added temporal jitter to the auditory metronome to determine whether participants would integrate auditory and tactile signals, with reduced weighting of the auditory metronome as its reliability decreased under bimodal conditions. We found that older adults matched the performance of young adults when synchronising to an isochronous auditory or tactile metronome. When the temporal regularity of the auditory metronome was reduced, older adults' performance was degraded to a greater extent than the young adults in both unimodal and bimodal conditions. However, proportionally both groups showed similar improvements in synchronisation performance in bimodal conditions compared with the equivalent, auditory-only conditions. We conclude that while older adults become more variable in synchronising to less regular beats, they do not show any deficit in the integration of multisensory temporal cues, suggesting that using multisensory information may help mitigate any deficits in coordinating actions to complex timing cues.

Combining multisensory temporal information for movement synchronisation.

The ability to synchronise actions with environmental events is a fundamental skill supporting a variety of group activities. In such situations, multiple sensory cues are usually available for synchronisation, yet previous studies have suggested that auditory cues dominate those from other modalities. We examine the control of rhythmic action on the basis of auditory and haptic cues and show that performance is sensitive to both sources of information for synchronisation. Participants were required to tap the dominant hand index finger in synchrony with a metronome defined by periodic auditory tones, imposed movements of the non-dominant index finger, or both cues together. Synchronisation was least variable with the bimodal metronome as predicted by a maximum likelihood estimation (MLE) model. However, increases in timing variability of the auditory cue resulted in some departures from the MLE model. Our findings indicate the need for further investigation of the MLE account of the integration of multisensory signals in the temporal control of action.

Unitary haptic perception: integrating moving tactile inputs from anatomically adjacent and non-adjacent digits.

How do we achieve unitary perception of an object when it touches two parts of the sensory epithelium that are not contiguous? We investigated this problem with a simple psychophysical task, which we then used in an fMRI experiment. Two wooden rods were moved over two digits positioned to be spatially adjacent. The digits were either from one foot (or hand) or one digit was from either foot (or hand). When the rods were moving in phase, one object was reliably perceived. By contrast, when the rods were moving out of phase, two objects were reliably perceived. fMRI revealed four cortical areas where activity was higher when the moving rods were perceived as one object relative to when they were perceived as two separate objects. Areas in the right inferior parietal lobule, the left inferior temporal sulcus and the left middle frontal gyrus were activated for this contrast regardless of the anatomical configuration of the stimulated sensory epithelia. By contrast, the left intraparietal sulcus was activated specifically when integration across the midline was required, irrespective of whether the stimulation was applied to the hands or feet. These results reveal a network of brain areas involved in generating a unified percept of the presence of an object that comes into contact with different parts of the body surface.

Contact forces in roughness discrimination.

Roughness perception through fingertip contact with a textured surface can involve spatial and temporal cues from skin indentation and vibration respectively. Both types of cue may be affected by contact forces when feeling a surface and we ask whether, on a given trial, discrimination performance relates to contact forces. We examine roughness discrimination performance in a standard psychophysical method (2-interval forced choice, in which the participant identifies which of two spatial textures formed by parallel grooves feels rougher) while continuously measuring the normal and tangential forces applied by the index finger. Fourteen participants discriminated spatial gratings in fine (spatial period of 320-580 micron) and coarse (1520-1920 micron) ranges using static pressing or sliding contact of the index finger. Normal contact force (mean and variability) during pressing or sliding had relatively little impact on accuracy of roughness judgments except when pressing on surfaces in the coarse range. Discrimination was better for sliding than pressing in the fine but not the coarse range. In contrast, tangential force fluctuations during sliding were strongly related to roughness judgment accuracy.