SciCombinator

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Concept: Proprioception

662

Brain-machine interfaces (BMIs) provide a new assistive strategy aimed at restoring mobility in severely paralyzed patients. Yet, no study in animals or in human subjects has indicated that long-term BMI training could induce any type of clinical recovery. Eight chronic (3-13 years) spinal cord injury (SCI) paraplegics were subjected to long-term training (12 months) with a multi-stage BMI-based gait neurorehabilitation paradigm aimed at restoring locomotion. This paradigm combined intense immersive virtual reality training, enriched visual-tactile feedback, and walking with two EEG-controlled robotic actuators, including a custom-designed lower limb exoskeleton capable of delivering tactile feedback to subjects. Following 12 months of training with this paradigm, all eight patients experienced neurological improvements in somatic sensation (pain localization, fine/crude touch, and proprioceptive sensing) in multiple dermatomes. Patients also regained voluntary motor control in key muscles below the SCI level, as measured by EMGs, resulting in marked improvement in their walking index. As a result, 50% of these patients were upgraded to an incomplete paraplegia classification. Neurological recovery was paralleled by the reemergence of lower limb motor imagery at cortical level. We hypothesize that this unprecedented neurological recovery results from both cortical and spinal cord plasticity triggered by long-term BMI usage.

Concepts: Spinal cord, Sensory system, Sense, Somatosensory system, Spinal cord injury, Virtual reality, Proprioception, Paraplegia

228

Social touch plays a powerful role in human life, with important physical and mental health benefits in development and adulthood. Touch is central in building the foundations of social interaction, attachment, and cognition [1-5], and early, social touch has unique, beneficial neurophysiological and epigenetic effects [6-9]. The recent discovery of a separate neurophysiological system for affectively laden touch in humans has further kindled scientific interest in the area [10, 11]. Remarkably, however, little is known about what motivates and sustains the human tendency to touch others in a pro-social manner. Given the importance of social touch, we hypothesized that active stroking elicits more sensory pleasure when touching others' skin than when touching one’s own skin. In a set of six experiments (total N = 133) we found that healthy participants, mostly tested in pairs to account for any objective differences in skin softness, consistently judged another’s skin as feeling softer and smoother than their own skin. We further found that this softness illusion appeared selectively when the touch activated a neurophysiological system for affective touch in the receiver. We conclude that this sensory illusion underlies a novel, bodily mechanism of socio-affective bonding and enhances our motivation to touch others.

Concepts: Psychology, Human, Sensory system, Skin, Sense, Somatosensory system, Emotion, Proprioception

187

Background The senses of touch and proprioception evoke a range of perceptions and rely on the ability to detect and transduce mechanical force. The molecular and neural mechanisms underlying these sensory functions remain poorly defined. The stretch-gated ion channel PIEZO2 has been shown to be essential for aspects of mechanosensation in model organisms. Methods We performed whole-exome sequencing analysis in two patients who had unique neuromuscular and skeletal symptoms, including progressive scoliosis, that did not conform to standard diagnostic classification. In vitro and messenger RNA assays, functional brain imaging, and psychophysical and kinematic tests were used to establish the effect of the genetic variants on protein function and somatosensation. Results Each patient carried compound-inactivating variants in PIEZO2, and each had a selective loss of discriminative touch perception but nevertheless responded to specific types of gentle mechanical stimulation on hairy skin. The patients had profoundly decreased proprioception leading to ataxia and dysmetria that were markedly worse in the absence of visual cues. However, they had the ability to perform a range of tasks, such as walking, talking, and writing, that are considered to rely heavily on proprioception. Conclusions Our results show that PIEZO2 is a determinant of mechanosensation in humans. (Funded by the National Institutes of Health Intramural Research Program.).

Concepts: Protein, Messenger RNA, Action potential, Perception, Sensory system, Sense, Somatosensory system, Proprioception

187

Increasing evidence suggests that the basic foundations of the self lie in the brain systems that represent the body. Specific sensorimotor stimulation has been shown to alter the bodily self. However, little is known about how disconnection of the brain from the body affects the phenomenological sense of the body and the self. Spinal cord injury (SCI) patients who exhibit massively reduced somatomotor processes below the lesion in the absence of brain damage are suitable for testing the influence of body signals on two important components of the self-the sense of disembodiment and body ownership. We recruited 30 SCI patients and 16 healthy participants, and evaluated the following parameters: (i) depersonalization symptoms, using the Cambridge Depersonalization Scale (CDS), and (ii) measures of body ownership, as quantified by the rubber hand illusion (RHI) paradigm. We found higher CDS scores in SCI patients, which show increased detachment from their body and internal bodily sensations and decreasing global body ownership with higher lesion level. The RHI paradigm reveals no alterations in the illusory ownership of the hand between SCI patients and controls. Yet, there was no typical proprioceptive drift in SCI patients with intact tactile sensation on the hand, which might be related to cortical reorganization in these patients. These results suggest that disconnection of somatomotor inputs to the brain due to spinal cord lesions resulted in a disturbed sense of an embodied self. Furthermore, plasticity-related cortical changes might influence the dynamics of the bodily self.

Concepts: Nervous system, Brain, Sensory system, Sense, Cerebrospinal fluid, Neural tube, Proprioception, Physical trauma

183

While the different sensory modalities are sensitive to different stimulus energies, they are often charged with extracting analogous information about the environment. Neural systems may thus have evolved to implement similar algorithms across modalities to extract behaviorally relevant stimulus information, leading to the notion of a canonical computation. In both vision and touch, information about motion is extracted from a spatiotemporal pattern of activation across a sensory sheet (in the retina and in the skin, respectively), a process that has been extensively studied in both modalities. In this essay, we examine the processing of motion information as it ascends the primate visual and somatosensory neuraxes and conclude that similar computations are implemented in the two sensory systems.

Concepts: Retina, Visual system, Sensory system, Skin, Sense, Somatosensory system, Proprioception, Stimulus modality

183

The sense of body ownership represents a fundamental aspect of our self-consciousness. Influential experimental paradigms, such as the rubber hand illusion (RHI), in which a seen rubber hand is experienced as part of one’s body when one’s own unseen hand receives congruent tactile stimulation, have extensively examined the role of exteroceptive, multisensory integration on body ownership. However, remarkably, despite the more general current interest in the nature and role of interoception in emotion and consciousness, no study has investigated how the illusion may be affected by interoceptive bodily signals, such as affective touch. Here, we recruited 52 healthy, adult participants and we investigated for the first time, whether applying slow velocity, light tactile stimuli, known to elicit interoceptive feelings of pleasantness, would influence the illusion more than faster, emotionally-neutral, tactile stimuli. We also examined whether seeing another person’s hand vs. a rubber hand would reduce the illusion in slow vs. fast stroking conditions, as interoceptive signals are used to represent one’s own body from within and it is unclear how they would be integrated with visual signals from another person’s hand. We found that slow velocity touch was perceived as more pleasant and it produced higher levels of subjective embodiment during the RHI compared with fast touch. Moreover, this effect applied irrespective of whether the seen hand was a rubber or a confederate’s hand. These findings provide support for the idea that affective touch, and more generally interoception, may have a unique contribution to the sense of body ownership, and by implication to our embodied psychological “self.”

Concepts: Perception, Sensory system, Sense, Somatosensory system, Proprioception, Feeling, Illusion, Pleasure

174

In anorexia nervosa (AN), body distortions have been associated with parietal cortex (PC) dysfunction. The PC is the anatomical substrate for a supramodal reference framework involved in spatial orientation constancy. Here, we sought to evaluate spatial orientation constancy and the perception of body orientation in AN patients. In the present study, we investigated the effect of passive lateral body inclination on the visual and tactile subjective vertical (SV) and body Z-axis in 25 AN patients and 25 healthy controls. Subjects performed visual- and tactile-spatial judgments of axis orientations in an upright position and tilted 90° clockwise or counterclockwise. We observed a significant deviation of the tactile and visual SV towards the body (an A-effect) under tilted conditions, suggesting a multisensory impairment in spatial orientation. Deviation of the Z-axis in the direction of the tilt was also observed in the AN group. The greater A-effect in AN patients may reflect reduced interoceptive awareness and thus inadequate consideration of gravitational inflow. Furthermore, marked body weight loss could decrease the somatosensory inputs required for spatial orientation. Our study results suggest that spatial references are impaired in AN. This may be due to particular integration of visual, tactile and gravitational information (e.g. vestibular and proprioceptive cues) in the PC.

Concepts: Anorexia nervosa, Sensory system, Sense, Somatosensory system, Orientation, Parietal lobe, Proprioception, Axial tilt

173

Our body feels like it is ours. However, individuals with body integrity identity disorder (BIID) lack this feeling of ownership for distinct limbs and desire amputation of perfectly healthy body parts. This extremely rare condition provides us with an opportunity to study the neural basis underlying the feeling of limb ownership, since these individuals have a feeling of disownership for a limb in the absence of apparent brain damage. Here we directly compared brain activation between limbs that do and do not feel as part of the body using functional MRI during separate tactile stimulation and motor execution experiments. In comparison to matched controls, individuals with BIID showed heightened responsivity of a large somatosensory network including the parietal cortex and right insula during tactile stimulation, regardless of whether the stimulated leg felt owned or alienated. Importantly, activity in the ventral premotor cortex depended on the feeling of ownership and was reduced during stimulation of the alienated compared to the owned leg. In contrast, no significant differences between groups were observed during the performance of motor actions. These results suggest that altered somatosensory processing in the premotor cortex is associated with the feeling of disownership in BIID, which may be related to altered integration of somatosensory and proprioceptive information.

Concepts: Brain, Cerebral cortex, Cerebrum, Sense, Somatosensory system, Premotor cortex, Proprioception, Ventral spinocerebellar tract

167

Following the amputation of a limb, many amputees report that they can still vividly perceive its presence despite conscious knowledge that it is not physically there. However, our ability to probe the mental representation of this experience is limited by the intractable and often distressing pain associated with amputation. Here, we present a method for eliciting phantom-like experiences in non-amputees using a variation of the rubber hand illusion in which a finger has been removed from the rubber hand. An interpretative phenomenological analysis revealed that the structure of this experience shares a wide range of sensory attributes with subjective reports of phantom limb experience. For example, when the space where the ring finger should have been on the rubber hand was stroked, 93% of participants (i.e., 28/30) reported the vivid presence of a finger that they could not see and a total of 57% (16/28) of participants who felt that the finger was present reported one or more additional sensory qualities such as tingling or numbness (25%; 7/28) and alteration in the perceived size of the finger (50%; 14/28). These experiences indicate the adaptability of body experience and share some characteristics of the way that phantom limbs are described. Participants attributed changes to the shape and size of their “missing” finger to the way in which the experimenter mimed stroking in the area occupied by the missing finger. This alteration of body perception is similar to the phenomenon of telescoping experienced by people with phantom limbs and suggests that our sense of embodiment not only depends on internal body representations but on perceptual information coming from peripersonal space.

Concepts: Perception, Sense, Mind, Amputation, Proprioception, Philosophy of perception, Phantom limb, Illusion

161

Restoration of touch after hand amputation is a desirable feature of ideal prostheses. Here, we show that texture discrimination can be artificially provided in human subjects by implementing a neuromorphic real-time mechano-neuro-transduction (MNT), which emulates to some extent the firing dynamics of SA1 cutaneous afferents. The MNT process was used to modulate the temporal pattern of electrical spikes delivered to the human median nerve via percutaneous microstimulation in four intact subjects and via implanted intrafascicular stimulation in one transradial amputee. Both approaches allowed the subjects to reliably discriminate spatial coarseness of surfaces as confirmed also by a hybrid neural model of the median nerve. Moreover, MNT-evoked EEG activity showed physiologically plausible responses that were superimposable in time and topography to the ones elicited by a natural mechanical tactile stimulation. These findings can open up novel opportunities for sensory restoration in the next generation of neuro-prosthetic hands.

Concepts: Sensory system, Somatosensory system, Amputation, Star Trek: The Next Generation, Prosthesis, Proprioception, Hand, Thumb