Interfacing the Somatosensory System to Restore Touch and Proprioception: Essential Considerations

ABSTRACT

State-of-the-art upper extremity prostheses include anthropomorphic hands with dexterity that approximates that of a human. To be fully useful, these devices will require an advanced somatosensory neural interface to convey tactile and proprioceptive feedback to the user. To this end, microstimulation methods are being developed using microelectrode arrays implanted at various locations along the somatosensory neuraxis, from peripheral nerves to primary somatosensory cortex. There is presently no consensus as to the best approach, although results from animal and human studies lend support for each. The purpose of this review is to outline practical considerations for the design of a somatosensory interface based on present knowledge of the anatomy and physiology, prior attempts to elicit somatic sensations using electrical stimulation, and lessons learned from successful sensory neuroprostheses such as the cochlear implant.     

Experiencing the Cross-Sensory Error Signal During Movement Leads to Proprioceptive Recalibration

Abstract

Reaching to targets in a virtual reality environment with misaligned visual feedback of the hand results in changes in movements (visuomotor adaptation) and sense of felt hand position (proprioceptive recalibration). We asked if proprioceptive recalibration arises even when the misalignment between visual and proprioceptive estimates of hand position is only experienced during movement. Participants performed a “shooting task” through the targets with a cursor that was rotated 30° clockwise relative to hand motion. Results revealed that, following training on the shooting task, participants adapted their reaches to all targets by approximately 16° and recalibrated their sense of felt hand position by 8°. Thus, experiencing a sensory misalignment between visual and proprioceptive estimates of hand position during movement leads to proprioceptive recalibration.     

Rubber hands feel the touch of light

Two experiments involving a total of 220 subjects are reported. The experiments document that "stroking" a false hand with the bright beam of light from a laser pointer can produce tactile and thermal sensations when the hand can be seen as one's own. Overall, 66% of subjects reported somatic sensations from the light. Felt hand location was recalibrated toward the location of the false hand for those subjects who felt the light. Moreover, the proprioceptive recalibration from the laser experience was comparable to that produced by actual coordinated brushing of the false hand and of the unseen real hand after 2 min of stimulation. The illusion may be experienced on one's real hand as well. The results are discussed in terms of multisensory integration.     

Visuomotor Adaptation and Proprioceptive Recalibration

ABSTRACT

Motor learning, in particular motor adaptation, is driven by information from multiple senses. For example, when arm control is faulty, vision, touch, and proprioception can all report on the arm's movements and help guide the adjustments necessary for correcting motor error. In recent years we have learned a lot about how the brain integrates information from multiple senses for the purpose of perception. However, less is known about how multisensory data guide motor learning. Most models of, and studies on, motor learning focus almost exclusively on the ensuing changes in motor performance without exploring the implications on sensory plasticity. Nor do they consider how discrepancies in sensory information (e.g., vision and proprioception) related to hand position may affect motor learning. Here, we discuss research from our lab and others that shows how motor learning paradigms affect proprioceptive estimates of hand position, and how even the mere discrepancy between visual and proprioceptive feedback can affect learning and plasticity. Our results suggest that sensorimotor learning mechanisms do not exclusively rely on motor plasticity and motor memory, and that sensory plasticity, in particular proprioceptive recalibration, plays a unique and important role in motor learning.     

Perceiving one’s own movements when using a tool

The present study examined what participants perceive of their hand movements when using a tool. In the experiments different gains for either the x-axis or the y-axis perturbed the relation between hand movements on a digitizer tablet and cursor movements on a display. As a consequence of the perturbation participants drew circles on the display while their covered hand movements followed either vertical or horizontal ellipses on the digitizer tablet. When asked to evaluate their hand movements, participants were extremely uncertain about their trajectories. By varying the amount of visual feedback, findings indicated that the low awareness of one’s own movements originated mainly from an insufficient quality of the humans’ tactile and proprioceptive system or from an insufficient spatial reconstruction of this information in memory.     

An internal focus of attention is optimal when congruent with afferent proprioceptive task information

Whilst benefits of an external focus are shown to govern several characteristics of skill execution, specificity theory indicates that sources of afferent information most useful to performance execution are typically prioritised during processing.ObjectivesWe investigated whether an internal focus facilitates performance when pertinent afferent information is proprioceptive in nature and congruent with attentional focus. We also considered whether the mechanisms behind attentional focus differences are attributable to planning processes or online motor control.DesignExperiments 1 and 2 adopted a randomised design, whilst experiment 3 used a repeated measures approach.MethodIn Experiment 1 we investigated movement variability as a measure of planning and error correction under external and internal focus conditions in an aiming task. Experiment 2 removed visual information to increase pertinence of proprioceptive feedback for movement execution and Experiment 3 adopted a leg-extension task, where proprioceptive salience was enhanced using an ankle weight. We hypothesised that this would increase congruency between internal focus instructions and movement production.ResultsExperiments 1 and 2 revealed reduced amplitude errors under an internal focus whilst Experiment 3 showed similar findings with the addition of lower EMG activity when adopting an internal focus. Movement variability findings were indicative of enhanced planning.ConclusionsWhen pertinence of proprioceptive information was amplified, benefits of an internal focus were more pronounced and performance was higher. Participants were better able to focus on movement characteristics to process proprioceptive feedback: something not afforded under an external focus. This raises doubts regarding the rigidity of the constrained action hypothesis.     

Sensory feedback in the learning of a novel motor task

The role of different forms of feedback is examined in learning a novel motor task. Five groups of ten subjects had to learn the voluntary control of the abduction of the big toe, each under a different feedback condition (proprioceptive feedback, visual feedback, EMG feedback, tactile feedback, force feedback). The task was selected for two reasons. First, in most motor learning studies subjects have to perform simple movements which present hardly any learning problem. Second, studying the learning of a new movement an provide useful information for neuromuscular reeducation, where patients often also have to learn movements for which no control strategy exists. The results show that artificial sensory feedback (EMG feedback, force feedback) is more powerful than "natural" (proprioceptive, visual, and tactile) feedback. The implications of these results for neuromuscular reeducation are discussed.     

Sensory Feedback in the Learning of a Novel Motor Task

The role of different forms of feedback is examined in learning a novel motor task. Five groups of ten subjects had to learn the voluntary control of the abduction of the big toe, each under a different feedback condition (proprioceptive feedback, visual feedback, EMG feedback, tactile feedback, force feedback). The task was selected for two reasons. First, in most motor learning studies subjects have to perform simple movements which present hardly any learning problem. Second, studying the learning of a new movement can provide useful information for neuromuscular reeducation, where patients often also have to learn movements for which no control strategy exists. The results show that artificial sensory feedback (EMG feedback, force feedback) is more powerful than “natural” (proprioceptive, visual, and tactile) feedback. The implications of these results for neuromuscular reeducation are discussed.     

Occupational Therapy Assessment of Neurodevelopmentally Disordered Children and Adolescents

ABSTRACT

Research suggests that many children and adolescents with neurodevelopmental disorders such as attention deficit hyperactivity disorder or Tourette syndrome exhibit neurological soft signs including sensory misperception. The parents of 52 children or adolescents, ages 6 to 16, entering the Neurodevelopmental Disorders Clinic at St Boniface General Hospital completed a structured questionnaire measuring sensory and motor systems. The questionnaire formed the basis of a semi-structured interview involving parent(s) and child or adolescent. Results suggested altered sensory and motor processing and indicated an increased sensory sensitivity regarding tactile, auditory, olfactury, gustatory and visual sensations. The literature regarding sensory defensiveness and neurodevelopmental systems is discussed in relation to the findings from the sample.     

Roughness perception during the rubber hand illusion

Watching a rubber hand being stroked by a paintbrush while feeling identical stroking of one’s own occluded hand can create a compelling illusion that the seen hand becomes part of one’s own body. It has been suggested that this so-called rubber hand illusion (RHI) does not simply reflect a bottom–up multisensory integration process but that the illusion is also modulated by top–down, cognitive factors. Here we investigated for the first time whether the conceptual interpretation of the sensory quality of the visuotactile stimulation in terms of roughness can influence the occurrence of the illusion and vice versa, whether the presence of the RHI can modulate the perceived sensory quality of a given tactile stimulus (i.e., in terms of roughness). We used a classical RHI paradigm in which participants watched a rubber hand being stroked by either a piece of soft or rough fabric while they received synchronous or asynchronous tactile stimulation that was either congruent or incongruent with respect to the sensory quality of the material touching the rubber hand. (In)congruencies between the visual and tactile stimulation did neither affect the RHI on an implicit level nor on an explicit level, and the experience of the RHI in turn did not cause any modulations of the felt sensory quality of touch on participant’s own hand. These findings first suggest that the RHI seems to be resistant to top–down knowledge in terms of a conceptual interpretation of tactile sensations. Second, they argue against the hypothesis that participants own hand tends to disappear during the illusion and that the rubber hand actively replaces it.     

Active inference, sensory attenuation and illusions

Active inference provides a simple and neurobiologically plausible account of how action and perception are coupled in producing (Bayes) optimal behaviour. This can be seen most easily as minimising prediction error: we can either change our predictions to explain sensory input through perception. Alternatively, we can actively change sensory input to fulfil our predictions. In active inference, this action is mediated by classical reflex arcs that minimise proprioceptive prediction error created by descending proprioceptive predictions. However, this creates a conflict between action and perception; in that, self-generated movements require predictions to override the sensory evidence that one is not actually moving. However, ignoring sensory evidence means that externally generated sensations will not be perceived. Conversely, attending to (proprioceptive and somatosensory) sensations enables the detection of externally generated events but precludes generation of actions. This conflict can be resolved by attenuating the precision of sensory evidence during movement or, equivalently, attending away from the consequences of self-made acts. We propose that this Bayes optimal withdrawal of precise sensory evidence during movement is the cause of psychophysical sensory attenuation. Furthermore, it explains the force-matching illusion and reproduces empirical results almost exactly. Finally, if attenuation is removed, the force-matching illusion disappears and false (delusional) inferences about agency emerge. This is important, given the negative correlation between sensory attenuation and delusional beliefs in normal subjects—and the reduction in the magnitude of the illusion in schizophrenia. Active inference therefore links the neuromodulatory optimisation of precision to sensory attenuation and illusory phenomena during the attribution of agency in normal subjects. It also provides a functional account of deficits in syndromes characterised by false inference and impaired movement—like schizophrenia and Parkinsonism—syndromes that implicate abnormal modulatory neurotransmission.     

Affective touch modulates the rubber hand illusion

Introduction

Humans experience touch as pleasant when this occurs with a certain velocity (1–10cm/s). Affective, pleasant touch is thought to be mediated by a distinct neural pathway consisting of un-myelinated tactile afferents (C tactile fibers) that respond to stroking with a low velocity on the hairy skin. As pleasant touch provides additional information on bodily signals we hypothesized that, compared to regular touch, pleasant touch would have a stronger effect on body ownership as measured through induction of the rubber hand illusion (RHI).

Methods

Two experiments involving the RHI were conducted. In the first experiment, the effects of stroking velocity (3 cm/s and 30 cm/s) and stroking material (soft/rough) on the RHI were tested. In the second experiment, the effect of an additional stroking velocity (0.3 cm/s) and side of stimulation (hairy and glabrous) was examined.

Results

The first experiment showed that low velocity stroking in combination with a soft material was not only regarded as most pleasant but also resulted in an enhanced RHI on proprioceptive drift and temperature measurements. In the second experiment, we confirmed that stroking with a velocity of 3 cm/s resulted in a larger RHI in terms of proprioceptive drift. In addition, compared to regular touch, pleasant touch of the hairy skin resulted in a larger proprioceptive drift, while similar stroking on the glabrous side of the skin did not induce a stronger effect of RHI on proprioceptive drift.

Conclusion

Our data suggest that pleasant touch modulates the body representation which is consistently reflected in a larger proprioceptive drift. Our data also suggest that C tactile fibers are likely to be involved in the modulation of body ownership.     

II Sensory feedback influences on keytapping motor tasks

Subjects were trained to tap a key continuously at a specific rate, and with a specific amount of pressure (regularity task). Performance of this task was studied under conditions of: (a) decreased auditory feedback (masking noise through earphones), (b) decreased visual feedback (tapping hand screened from view), (c) vibration (vibrators applied to forearm in order to “mask” proprioceptive feedback), (d) digital block of tapping finger, and (e) combination of all four conditions. Significant changes in rate and intensity of tapping resulted under conditions of decreased auditory feedback, vibration, and the combined condition.

In the second part of the study, the effects of different delayed sensory events on keytapping were examined. The five conditions of delayed sensory feedback were: (a) delayed auditory feedback, (b) delayed visual feedback, (c) delayed tactile feedback, (d) the first three delayed sensory events presented simultaneously, and (e) condition (d) repeated with digital block of the tapping finger.

The conditions of delayed sensory feedback did not markedly alter performance of the regularity task. The same conditions of delayed sensory feedback did, however, produce highly significant changes in the performance of a more complex pattern task. All of these delay conditions produced parallel changes in the pattern task, namely increased intensity and decreased rate of tapping. The fact that the pattern task is more disturbed by delayed sensory feedback than the regularity task suggests that temporal complexity of the task is one determinant of the degree to which it will be disturbed by a delay in sensory feedback.     

Modeling body state-dependent multisensory integration

The brain often integrates multisensory sources of information in a way that is close to the optimal according to Bayesian principles. Since sensory modalities are grounded in different, body-relative frames of reference, multisensory integration requires accurate transformations of information. We have shown experimentally, for example, that a rotating tactile stimulus on the palm of the right hand can influence the judgment of ambiguously rotating visual displays. Most significantly, this influence depended on the palm orientation: when facing upwards, a clockwise rotation on the palm yielded a clockwise visual judgment bias; when facing downwards, the same clockwise rotation yielded a counterclockwise bias. Thus, tactile rotation cues biased visual rotation judgment in a head-centered reference frame. Recently, we have generated a modular, multimodal arm model that is able to mimic aspects of such experiments. The model co-represents the state of an arm in several modalities, including a proprioceptive, joint angle modality as well as head-centered orientation and location modalities. Each modality represents each limb or joint separately. Sensory information from the different modalities is exchanged via local forward and inverse kinematic mappings. Also, re-afferent sensory feedback is anticipated and integrated via Kalman filtering. Information across modalities is integrated probabilistically via Bayesian-based plausibility estimates, continuously maintaining a consistent global arm state estimation. This architecture is thus able to model the described effect of posture-dependent motion cue integration: tactile and proprioceptive sensory information may yield top-down biases on visual processing. Equally, such information may influence top-down visual attention, expecting particular arm-dependent motion patterns. Current research implements such effects on visual processing and attention.     

Modeling body state-dependent multisensory integration

The brain often integrates multisensory sources of information in a way that is close to the optimal according to Bayesian principles. Since sensory modalities are grounded in different, body-relative frames of reference, multisensory integration requires accurate transformations of information. We have shown experimentally, for example, that a rotating tactile stimulus on the palm of the right hand can influence the judgment of ambiguously rotating visual displays. Most significantly, this influence depended on the palm orientation: when facing upwards, a clockwise rotation on the palm yielded a clockwise visual judgment bias; when facing downwards, the same clockwise rotation yielded a counterclockwise bias. Thus, tactile rotation cues biased visual rotation judgment in a head-centered reference frame. Recently, we have generated a modular, multimodal arm model that is able to mimic aspects of such experiments. The model co-represents the state of an arm in several modalities, including a proprioceptive, joint angle modality as well as head-centered orientation and location modalities. Each modality represents each limb or joint separately. Sensory information from the different modalities is exchanged via local forward and inverse kinematic mappings. Also, re-afferent sensory feedback is anticipated and integrated via Kalman filtering. Information across modalities is integrated probabilistically via Bayesian-based plausibility estimates, continuously maintaining a consistent global arm state estimation. This architecture is thus able to model the described effect of posture-dependent motion cue integration: tactile and proprioceptive sensory information may yield top–down biases on visual processing. Equally, such information may influence top–down visual attention, expecting particular arm-dependent motion patterns. Current research implements such effects on visual processing and attention.     

Having a body versus moving your body: How agency structures body-ownership

We investigated how motor agency in the voluntary control of body movement influences body awareness. In the Rubber Hand Illusion (RHI), synchronous tactile stimulation of a rubber hand and the participant's hand leads to a feeling of the rubber hand being incorporated in the participant's own body. One quantifiable behavioural correlate of the illusion is an induced shift in the perceived location of the participant's hand towards the rubber hand. Previous studies showed that the induced changes in body awareness are local and fragmented: the proprioceptive drift is largely restricted to the stimulated finger. In the present study, we investigated whether active and passive movements, rather than tactile stimulation, would lead to similarly fragmented body awareness. Participants watched a projected image of their hand under three conditions: active finger movement, passive finger movement, and tactile stimulation. Visual feedback was either synchronous or asynchronous with respect to stimulation of the hand. A significant overall RHI, defined as greater drifts following synchronous than asynchronous stimulation, was found in all cases. However, the distribution of the RHI across stimulated and non-stimulated fingers depended on the kind of stimulation. Localised proprioceptive drifts, specific to the stimulated finger, were found for tactile and passive stimulation. Conversely, during active movement of a single digit, the proprioceptive drifts were not localised to that digit, but were spread across the whole hand. Whereas a purely proprioceptive sense of body-ownership is local and fragmented, the motor sense of agency integrates distinct body-parts into a coherent, unified awareness of the body.     

An interpretation of research of feedback interruption in speech.

The controversial question of the scope of sensory control in the voluntary motor patterns involved in speech is examined by reviewing studies in which the auditory, tactile, and proprioceptive feedback channels have been distorted or interrupted. The author makes a case for open loop control of well-learned speech patterns under normal circumstances. The concept of internal feedback is introduced as a possible control system of skilled speech, whereas response feedback and external feedback are viewed as necessary for children developing speech or adults learning new speech patterns.     

An interpretation of research on feedback interruption in speech

The controversial question of the scope of sensory control in the voluntary motor patterns involved in speech is examined by reviewing studies in which the auditory, tactile, and proprioceptive feedback channels have been distorted or interrupted. The author makes a case for open loop control of well-learned speech patterns under normal circumstances. The concept of internal feedback is introduced as a possible control system of skilled speech, whereas response feedback and external feedback are viewed as necessary for children developing speech or adults learning new speech patterns.     

Tactile orientation constancy: Do proprioception and attention affect the tactile vertical?1

Abstract: Tactile vertical, defined as the edge orientation that participants perceive to be vertical, was examined in four experiments. In Experiment 1, we touched the participants’ cheek, lips, or hand with an edge and asked them to judge its orientation with regard to gravitational vertical, both when the stimulated body part was upright (or, in the case of the lips, aligned), and when it was tilted (lips, distorted). We found that when the head or hand was tilted forward 30°, or when the lower lip was distorted approximately 38° to the left or right, the tactile vertical shifted in the same direction by only a fraction (8.7, 8.6, and 36.3% for the cheek, lips, and hand, respectively) of the change in orientation of the stimulated region. The results indicated considerable, but usually incomplete, orientation constancy. In Experiment 2, we measured tactile vertical on the hand for forward tilts from 0° to 45°. We found that as the hand was tilted, the tactile vertical increasingly shifted in the same direction as the hand (i.e., a tactile Aubert effect). In Experiment 3, the effect of attentional focus on tactile vertical was examined by comparing the tactile vertical of participants who attended to body‐centered coordinates, and others who attended to gravitation‐centered coordinates. We found that focusing on body‐centered coordinates caused a decrease in orientation constancy. We sought to examine the role of attention further in Experiment 4, measuring tactile vertical on the cheek of persons with temporomandibular disorders. Compared with normal participants, these participants displayed significantly lower constancy. The results were accounted for by a narrowing of attention to painful signals, so that proprioceptive information was attended to less. In conclusion, the degree of tactile orientation constancy that participants demonstrate varies as a function of body site and attentional focus.     

Planning Maximally Smooth Hand Movements Constrained to Nonplanar Workspaces

The article characterizes hand paths and speed profiles for movements performed in a nonplanar, 2-dimensional workspace (a hemisphere of constant curvature). The authors assessed endpoint kinematics (i.e., paths and speeds) under the minimum-jerk model assumptions and calculated minimal amplitude paths (geodesics) and the corresponding speed profiles. The authors also calculated hand speeds using the 2/3 power law. They then compared modeled results with the empirical observations. In all, 10 participants moved their hands forward and backward from a common starting position toward 3 targets located within a hemispheric workspace of small or large curvature. Comparisons of modeled observed differences using 2-way RM-ANOVAs showed that movement direction had no clear influence on hand kinetics (p < .05). Workspace curvature affected the hand paths, which seldom followed geodesic lines. Constraining the paths to different curvatures did not affect the hand speed profiles. Minimum-jerk speed profiles closely matched the observations and were superior to those predicted by 2/3 power law (p < .001). The authors conclude that speed and path cannot be unambiguously linked under the minimum-jerk assumption when individuals move the hand in a nonplanar 2-dimensional workspace. In such a case, the hands do not follow geodesic paths, but they preserve the speed profile, regardless of the geometric features of the workspace.