Tactile innervation densities across the whole body

Abstract

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

Mechanoreceptor synapses in the brainstem shape the central representation of touch

“…In this view, different skin regions uniquely instruct expansion of mechanoreceptor synapses in the brainstem to shape a collective central representation. This model reconciles previously observed discrepancies between innervation density and central representation across the body in multiple species and quantitatively fits our data for mouse hindlimb and forelimb glabrous and hairy skin (Catania and Kaas, 1997; Corniani and Saal, 2020; Lee and Woolsey, 1975). We propose that skin region dependent patterns and strengths of LTMR synaptic connections within the brainstem reduce evolutionary constraints by allowing body maps to be flexibly tailored to disparate mammalian body forms.…”

“…Multiple lines of evidence suggest that the central representation of touch is at least partly determined by skin innervation density (Lee and Woolsey, 1975; Corniani and Saal, 2020). Enrichment of sensory receptors in specific skin targets may reflect increased production of somatosensory neurons at the relevant axial levels, enhanced attraction of peripheral axonal projections, or decreased cell death of sensory neurons that innervate those skin regions, producing differences in innervation density.…”

“…For example, the primary somatosensory cortex and the superior colliculus contain body maps with differing proportions (Drager and Hubel, 1976), suggesting that the same peripheral inputs can support different central representations. Moreover, a recent compilation of human anatomical and physiological measurements argues that differences in peripheral sensory neuron numbers may not account for the over-representation of the hands and the digits in somatosensory cortex (Corniani and Saal, 2020). This parallels work in the visual system, where studies argue that increased photoreceptor density at the primate retinal fovea alone is insufficient to explain the enlarged representation of central fields of view in the visual cortex (Azzopardi and Cowey, 1993).…”

Probing interoception via thermosensation: No specific relationships across multiple interoceptive sub-modalities

“…Warm temperature detection was significantly correlated with both cold detection (Benjamini- Hochberg adjusted p value = 0.04) and pain (Benjamini-Hochberg adjusted p value = 0.01) detection in the palm, suggesting a relationship between the mechanisms of temperature and pain detection in the palm but not in the forearm. This could be due to the richer presence of fibres in hairy vs. non-hairy skin (Corniani and Saal, 2020) and thus – potentially - the presence of more separate mechanisms for the detection of temperature and pain in hairy skin compared to non-hairy skin.…”

“…If this is the case, thermal signals detected through the hairy skin of our body might have a privileged role in social thermoregulation, maintenance of homeostasis and ultimately survival (Morrison, 2016), suggesting that the CT afferents might work in concert with cold and warm receptors to perceive and signal deviations from their optimal firing temperature (i.e., 32°C). In contrast, we theorise that thermal signals detected through the non-hairy skin of our body (e.g., palm) might potentially have a more discriminatory role and they might therefore be important for experiencing the temperature of grasped objects, for instance, a role that is less related to thermoregulation and more to exploring the properties of external objects (Vallbo and Johansson, 1984; Johansson and Flanagan, 2009; Corniani and Saal, 2020). This is further supported by our findings showing that overall, improved performance in temperature perception on hairy skin was more consistent when the thermal stimuli were dynamic compared to that in response to static stimuli.…”