Concept: Somatosensory system
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.
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.
Little is known about the molecular mechanisms underlying mammalian touch transduction. To identify novel candidate transducers, we examined the molecular and cellular basis of touch in one of the most sensitive tactile organs in the animal kingdom, the star of the star-nosed mole. Our findings demonstrate that the trigeminal ganglia innervating the star are enriched in tactile-sensitive neurons, resulting in a higher proportion of light touch fibers and lower proportion of nociceptors compared to the dorsal root ganglia innervating the rest of the body. We exploit this difference using transcriptome analysis of the star-nosed mole sensory ganglia to identify novel candidate mammalian touch and pain transducers. The most enriched candidates are also expressed in mouse somatosesensory ganglia, suggesting they may mediate transduction in diverse species and are not unique to moles. These findings highlight the utility of examining diverse and specialized species to address fundamental questions in mammalian biology.
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.).
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.
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.”
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.
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.
Interactions among animals can result in complex sensory signals containing a variety of socially relevant information, including the number, identity, and relative motion of conspecifics. How the spatiotemporal properties of such evolving naturalistic signals are encoded is a key question in sensory neuroscience. Here, we present results from experiments and modeling that address this issue in the context of the electric sense, which combines the spatial aspects of vision and touch, with the temporal aspects of audition. Wave-type electric fish, such as the brown ghost knifefish, Apteronotus leptorhynchus, used in this study, are uniquely identified by the frequency of their electric organ discharge (EOD). Multiple beat frequencies arise from the superposition of the EODs of each fish. We record the natural electrical signals near the skin of a “receiving” fish that are produced by stationary and freely swimming conspecifics. Using spectral analysis, we find that the primary beats, and the secondary beats between them (“beats of beats”), can be greatly influenced by fish swimming; the resulting motion produces low-frequency envelopes that broaden all the beat peaks and reshape the “noise floor”. We assess the consequences of this motion on sensory coding using a model electroreceptor. We show that the primary and secondary beats are encoded in the afferent spike train, but that motion acts to degrade this encoding. We also simulate the response of a realistic population of receptors, and find that it can encode the motion envelope well, primarily due to the receptors with lower firing rates. We discuss the implications of our results for the identification of conspecifics through specific beat frequencies and its possible hindrance by active swimming.
INTRODUCTION: Patients often complain about sensory symptoms that appear to the doctor as harmless, and reassurances are often given. Sensory strokes may easily be ignored. CASE PRESENTATION: A 48-year-old Caucasian woman with insulin-dependent diabetes and hyperlipidemia experienced symptoms that progressed within hours to a complete left-sided hemisensory syndrome. This was caused by a lacunar infarct in the ventral posterior tier nuclei of the right thalamus. A few days later she gradually developed an almost identical, but incomplete hemisensory syndrome on the opposite side caused by a corresponding lacune in the left thalamus. Severe persistent and paroxysmal pain on both sides of the body became disabling. CONCLUSION: Small strokes only affecting the somatosensory system should not be underestimated. Neuropathic pain may result. Probably unique in the present case is the demonstration of bilateral thalamic pain secondary to two almost identical thalamic infarcts. Small vessel disease (microatheroma or lipohyalinosis) was the most likely cause of the lacunes. One can only speculate if there was an occlusion in two separate thalamic perforators, or in a single dominant artery supplying the bilateral thalami.