The skin is our largest sensory organ and innervated by afferent fibers carrying tactile information to the spinal cord and onto the brain. The density with which different classes of tactile afferents innervate the skin is not constant but varies considerably across different body regions. However, precise estimates of innervation density are only available for some body parts, such as the hands, and estimates of the total number of tactile afferent fibers are inconsistent and incomplete. Here we reconcile different estimates and provide plausible ranges and best estimates for the number of different tactile fiber types innervating different regions of the skin, using evidence from dorsal root fiber counts, microneurography, histology, and psychophysics. We estimate that the skin across the whole body of young adults is innervated by approximately 230,000 tactile afferent fibers (plausible range: 200,000-270,000), with a subsequent decrement of 5-8% every decade due to aging. 15% of fibers innervate the palmar skin of both hands and 19% the region surrounding the face and lips. Slowly and fast-adapting fibers are split roughly evenly, but this breakdown varies with skin region. Innervation density correlates well with psychophysical spatial acuity across different body regions, and additionally, on hairy skin, with hair follicle density. Innervation density is also weakly correlated with the size of the cortical somatotopic representation, but cannot fully account for the magnification of the hands and the face.
The skin is our largest sensory organ and innervated by afferent fibers carrying tactile information to the spinal cord and onto the brain. The density with which different classes of tactile afferents innervate the skin is not constant but varies considerably across different body regions. However, precise estimates of innervation density are only available for some body parts, such as the hands, and estimates of the total number of tactile afferent fibers are inconsistent and incomplete. Here we reconcile different estimates and provide plausible ranges and best estimates for the number of different tactile fiber types innervating different regions of the skin, using evidence from dorsal root fiber counts, microneurography, histology, and psychophysics. We estimate that the skin across the whole body is innervated by approximately 230,000 tactile afferent fibers (plausible range: 200,000-270,000). 15% innervate the palmar skin of both hands and 19% the region surrounding the face and lips. Around 60% of all tactile fibers are slowly-adapting, while the rest are fastadapting. Innervation density correlates well with psychophysical spatial acuity across different body regions, and additionally, on hairy skin, with hair follicle density. Innervation density is also weakly correlated with the size of the cortical somatotopic representation, but cannot fully account for the magnification of the hands and the face. cutaneous afferent | mechanoreceptor | glabrous skin | hairy skin Correspondence: h.saal@sheffield.ac.uk Corniani et al. | bioRχiv | April 27, 2020 | 1-9
Sensory information is conveyed by populations of neurons, and coding strategies cannot always be deduced when considering individual neurons. Moreover, information coding depends on the number of neurons available and on the composition of the population when multiple classes with different response properties are available. Here, we study population coding in human tactile afferents by employing a recently developed simulator of mechanoreceptor firing activity. First, we highlight the interplay of afferents within each class. We demonstrate that the optimal afferent density to convey maximal information depends on both the tactile feature under consideration and the afferent class. Second, we find that information is spread across different classes for all tactile features and that each class encodes both redundant and complementary information with respect to the other afferent classes. Specifically, combining information from multiple afferent classes improves information transmission and is often more efficient than increasing the density of afferents from the same class. Finally, we examine the importance of temporal and spatial contributions, respectively, to the joint spatiotemporal code. On average, destroying temporal information is more destructive than removing spatial information, but the importance of either depends on the stimulus feature analysed. Overall, our results suggest that both optimal afferent innervation densities and the composition of the population depend in complex ways on the tactile features in question, potentially accounting for the variety in which tactile peripheral populations are assembled in different regions across the body.
The human fingertip can detect small tactile features with a spatial acuity roughly the width of a fingerprint ridge. However, how individual ridges deform under contact to support accurate and high-precision tactile feedback is currently unknown. The complex mechanical structure of the glabrous skin, composed of multiple layers and intricate morphology within which mechanoreceptors are embedded, makes this question challenging. Here, we used optical coherence tomography to image and track sub-surface deformations of hundreds of individual fingerprint ridges during contact events at high spatial resolution in vivo. We calculated strain patterns in both the stratum corneum and viable epidermis in response to a variety of tactile stimuli, including static indentation, stick-to-slip events, sliding of a flat surface in different directions, and interaction with small tactile features, such as edges and grooves. We found that ridges could stretch, compress, and undergo considerable shearing orthogonal to the skin surface, but there was limited horizontal shear. Therefore, it appears that the primary components of ridge deformation and, potentially, neural responses are deformations of the ridge flanks and their relative movement, rather than overall bending of the ridges themselves. We conclude that the local distribution of mechanoreceptors across the ridges might be ideally suited to extract the resulting strain gradients and that the fingertip skin may possess a higher mechanical spatial resolution than that of a single ridge.
Sensory information is conveyed by populations of neurons, and coding strategies cannot always be deduced when considering individual neurons. Moreover, information coding depends on the number of neurons available and on the composition of the population when multiple classes with different response properties are available. Here, we study population coding in human tactile afferents by employing a recently developed simulator of mechanoreceptor firing activity. First, we demonstrate that the optimal afferent density for conveying maximal information depends on the tactile feature under consideration and the afferent class coding this feature. Second, we find that information is spread across different classes for all tactile features, such that combining information from multiple afferent classes improves information transmission, and is often more efficient than increasing the density of afferents from the same class. Finally, we test the importance of timing precision and afferent identity in the population code to probe whether temporal and spatial information can be traded against each other. Destroying temporal information turns out to be more destructive than removing spatial information, and the contribution of either cannot be completely recovered from the other. Overall, our results suggest that both optimal afferent innervation densities and the composition of the population depend in complex ways on the tactile features in question, potentially accounting for the variety in which tactile peripheral populations are assembled in different regions across the body.
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