Evolution of Sensory Receptor Specializations inthe Glabrous Skin

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Evolution of Sensory Receptor Specializations in the Glabrous Skin

N J Dominy, University of California, Santa Cruz, CA, USA
2009 Elsevier Ltd. All rights reserved.

the adaptive function of glabrous skin and its associated receptors tends to vary according to the locomotor, foraging, and reproductive behaviors particular to a certain species.

Introduction
Glabrous skin is devoid of dermal filaments such as hair or feathers. It is prevalent among amphibians and reptiles and is characteristic of the maxillary rictus, interdigital web, and combs and wattles of birds. The glabrous skin of birds is lipogenic and sometimes temporary, e.g., brood (incubation) patches, or associated with the attainment of maturity. For instance, feather loss from the head is linked to maturation in some ibises and storks. Glabrous skin is more variable among mammals. The rhinarium, lips, and genitals are glabrous, as well as parts of limb extremities in contact with the physical environment during locomotion, such as the flippers of seals and sea lions and the cutaneous pads of paws. A patch of glabrous skin also exists on the prehensile tails of atelid monkeys and certain other arboreal mammals. Such animals typically suspend their bodies by way of their tail when moving or foraging on terminal branches. More specialized examples of glabrous skin include the nasal rays of the star-nosed mole, Condylura cristata, and the upper bill of the platypus, Ornithorhynchus anatinus, which is an extension of skin that covers much of the face. At the proximal end of the lower bill is a similar extension that folds over the neck. These areas are termed upper and lower shields, respectively. Glabrous skin is a major organ for sensing the external environment. Sensation from the glabrous skin along with sensations from hirsute skin, muscles, tendons, joints, and bones is termed somatic sensation. It is initiated by a variety of specialized receptors, many of which have structurally elaborate terminals that transform specific stimuli into nervous impulses. The sensory terminal may be encapsulated or linked to mesodermal or ectodermal elements. The extraneural cells are not necessarily excitable, but rather create the right circumstances for the excitation of the neuronal dendrite or modify its excitation in some way. Some receptors are remarkably uniform across vertebrate and mammalian orders, although considerable variation exists in the numbers of sensory receptors per square centimeter among the different areas of the body surface, and with advancing age the density of receptors can decrease. Not surprisingly,

Types of Cutaneous Receptors

The histological arrangement of a cutaneous receptor can differ greatly between hirsute and glabrous skin, as well as between animal species. This article has been written with a strong emphasis on the morphology and function of specialized receptors in the glabrous skin of mammals, which includes free nerve endings (FNEs), Merkel cells, Meissner corpuscles, Ruffini corpuscles, and Pacinian and paciniform corpuscles. Before the availability of electron microscopy, several other lamellar receptors were recognized (e.g., Golgi-Mazzoni and Dogiel corpuscles). However, they all follow the lamellar design pattern of the paciniform receptor and are considered part of this group. When stimulation of a cutaneous receptor is maintained at a steady level, there is, as in all receptors, an initial burst the dynamic phase followed by gradual habituation to that steady level the static phase. Although all receptors evince these two phases, one or the other predominates, giving a distinction between rapidly adapting (RA) endings that accurately record the rate of stimulus onset and slowly adapting (SA) endings that signal the constant amplitude of a stimulus, for example, the position sense. SA endings are further classified by the regularity of their discharge properties (type I and type II).
Free Nerve Endings

FNEs are the terminal receptor structures of sensory C-fibers or Ad fibers. FNEs are found in all connective tissues, including the epidermis and dermis of hirsute and glabrous skin. Afferent fibers are myelinated or nonmyelinated but are always of small diameter and low conduction velocity. The terminal arborizations of myelinated afferent axons are nonmyelinated and devoid of Schwann cell investment. Electrophysiological recordings of FNEs in the dermis show that they respond to several sensory modalities. Some FNEs respond to moderate cold or heat (thermoreception), to low-threshold mechanical touch (mechanoreception), or to damaging heat, cold, or deformation (nociception). The FNEs of afferent fibers are mainly nociceptive in the nonmyelinated portion. The lips and palms of primates feature an abundance of nonmyelinated C-fibers and a paucity of finely

40 Evolution of Sensory Receptor Specializations inthe Glabrous Skin

myelinated Ad fibers, which together give glabrous skin a lower heat detection threshold and a higher heat pain threshold than hirsute skin. This condition is hypothesized to enhance the function of glabrous skin as an exploratory surface. The exploratory function of glabrous skin is exemplified by the nasal rays of the star-nosed mole, Condylura cristata, which are richly invested with Eimers organs and are the moles primary sense organs. Named after the German zoologist Gustav Heinrich Theodor Eimer (18431898), Eimers organs are a special form of FNE found in the rhinarium of fossorial mammals such as talpid moles. In this structure, the FNE extends through a column of thickened epidermal cells. Below the column are Merkel cell complexes and lamellated paciniform corpuscle. The presence of three types of specialized receptor raises the possibility that Eimers organs have several important functions. The primary function appears to be the tactile detection and recognition of invertebrate prey, but the presence of up to three paciniform corpuscles at the base of each Eimers organ suggests that it may also play a role in sensing seismic vibrations. Such vibrations are important signals of communication between moles. The importance of FNEs for sensing prey is also evident in the infrared pit organs of snakes. In the rattlesnake, Crotalus horridus, the morphology of the pit organ promotes efficient thermoreception by a large number (several thousand) of intradermal myelinated axons 316 mm in diameter.
The Merkel Cell System

Although direct evidence is lacking, correlative electrophysiological and morphological evidence suggests that Merkel cells function as SA type I mechanoreceptors. Calcium ions enter the cell in response to maintained mechanical stimuli and trigger the release of a neurotransmitter, probably glutamate. The conserved morphology and widespread distribution of Merkel cells across such divergent animals as lizards, salamanders, and lampreys suggests an early appearance during vertebrate evolution. The adaptive significance appears to be associated with generalized somatosensory reception, particularly of prey objects. They are most sensitive to perpendicular deformation of the skin surface or to the bending of sinus hairs or vibrissae. Furthermore, the density of Merkel cells is manifested most strikingly in structures associated with foraging, such as the electroreceptive snouts of the platypus and echidna and the mystacial skin of most mammals, except humans. An association with foraging is also evident in the beak skin of birds, where Merkel-like cells occur in dense corpuscles containing up to 50 cells. The corpuscles, termed Grandry corpuscles, are present in the glabrous skin of the bill and tongue of wading birds but absent in the domestic chicken and Japanese quail. A structural resemblance of Grandry corpuscles to Merkel cells points to analogous functions, but they are not morphologically identical, and some evidence suggests that Grandry corpuscles function as RA receptors. The functional and ecological significance of such differences awaits elucidation.
The Meissner Corpuscle

Friedrich Sigmund Merkel (18451919) was an outstanding German anatomist of the late nineteenth century. He described cells in the skin of amphibians, birds, and mammals and referred to them as Tastzellen, or touch cells. The cells were given the eponym Merkel cells in 1878 by Robert Bonnet (18511921). Distinctive traits include dense core vesicles, cytoplasmic projections, and synaptiform contacts with enlarged nerve terminals. They measure 1015 mm across and exist in the dermis of birds and the basal layer of the epidermis of mammals. In mammals, Merkel cells are a ubiquitous component of both hirsute and glabrous skin. The myelinated afferent fiber branches extensively in the dermis within 500 mm of the epidermis. The branches lose their myelin sheaths before they penetrate the basement membrane of the epidermis to form the flattened nerve plate (Merkel disk) lying along the lower border of the Merkel cell. The disk itself is c. 7 mm in diameter and 1 mm thick and contains numerous mitochondria, which occupy 50% of the terminal. Merkel disks exist only in adult mammals.

Georg Meissner (18291905) was a German anatomist and physiologist of the nineteenth century. He and Rudolf Wagner (18051864) described distinctive corpuscles in 1852, which became the subject of a monograph by Meissner in 1853. This monograph is the basis for Meissners name being associated with the receptor. Meissner corpuscles are located in the dermal papillae of glabrous skin, where they connect to and tightly abut the basal surface of the epidermis. They are innervated by one or two myelinated fibers from the subepidermal nerve plexus. The fibers lose their myelination before entering the corpuscle, an ovoid capsule of perineural cells. Therein the nerve endings branch repeatedly, adopting a ribbonlike shape with bulbous expansions. Collagen fibers and fibrocytes bond the spiraling nerve endings to stacks of lamellar Schwann cells and attach the capsule to the epidermis. The circumscribed expansion of unmyelinated nerve endings into lamellar disks is a distinctive feature of Meissner corpuscles.

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Such complex innervation has led to speculation that Meissner corpuscles have a nociceptive function, although aspects of the disciform expansion suggest a primary role in mechanoreception. TakahashiIwanaga and Shimoda reported that the disk margins are serrated with fine projections of lamellar Schwann cells that tightly hold the collagen trabeculae to the inner aspect of the pericorpuscular capsule. They concluded that the disks are susceptible to mechanical deformations of surrounding tissues and, furthermore, that the distortion of axonal endings during the dynamic phase of tissue deformation will generate RA receptor potentials. Castano et al. observed that the minutest deformation of the skin [can be] immediately transmitted to the capsule and, via the cross-beam system linking it to the framework, to the transducer elements of the corpuscle (1985: 296). The disciform expansion is thus well suited to mechanotransduction. On this basis, Meissner corpuscles are hypothesized to play a key role in the perception of elastic texture. They are classified as RA receptors that respond to transient or phasic stimuli. They are particularly sensitive to vibrations at frequencies ranging from 10 to 400 Hz with maximum sensitivity between 100 and 200 Hz. Meissner corpuscles are reported from the glabrous skin of the lips and extremities (hands, feet, and prehensile tails) of primates and one marsupial, the Virginia opossum, Didelphis virginiana. Murine and sciurid corpuscles are similar in shape, but smaller and less elaborate. The high concentration of Meissner corpuscles at the tips of primate digits as well as the glabrous patch of skin present on the prehensile tail of atelid monkeys suggest that they function to sense the elastic properties of support structures, which has adaptive value in an arboreal milieu. An additional hypothesis is that the concentration of Meissner corpuscles at the digits supports the perception of food texture, particularly ripening fruits, which are often palpated by foraging primates. Hoffman et al. reported that the density of Meissner corpuscles in primate digits varied positively as a function of the overall proportion of fruit in the diet. In general, the function of Meissner corpuscles appears to be related to sensing the texture of critical objects in the environment the paucity of Meissner corpuscles in other mammalian orders is curious.
Pacinian Corpuscle

Filippo Pacini (181283) was an Italian anatomist posthumously famous for isolating the cholera bacillus Vibrio cholerae in 1854. Pacinian corpuscles, however, were first described by Abraham Vater (16841751) in 1741 and were rediscovered by Pacini

almost 100 years later in 1840. Pacinian corpuscles are the largest and best-known corpuscles in mammals. They are oval, spherical, or irregularly coiled and are exceptionally large, up to 2 mm in length and 100500 mm wide. Each has a capsule formed by c. 30 concentrically arranged lamellae of flat cells about 0.2 mm thick. Pacinian corpuscles are located in the palmar and plantar aponeurosis or genitalia deep to the skin. They are also present in ligaments and joint capsules of mammals and ostriches and the mesentery of the cat intestine where they are visible to the unaided eye. The afferent nerve fibers are myelinated with diameters between 3 and 6 mm. Extensive studies show these endings to behave as RA mechanoreceptors responding to sudden disturbances and vibrations (401000 Hz), with an optimal response at the higher end of the range. The widespread distribution of Pacinian and paciniform corpuscles throughout the body makes it difficult to assign an adaptive significance to their presence in glabrous skin. Yet attendant associations between paciniform corpuscles and specialized structures such as Eimers organs and the push rods of monotremes suggest that paciniform corpuscles are sometimes recruited for specialized roles. The push rod is a structure unique to the glabrous snout of the echidna, Tachyglossus aculeatus, and the upper and lower shields of the platypus, Ornithorhynchus anatinus. It is composed of a column of flattened spinous cells, which are cross-linked by tight junctions. The tip of the rod emerges at the skin surface with a domelike projection. The base of the push rod resembles an Eimers organ in that it is associated with Merkel cell complexes and lamellated paciniform corpuscles. The rod is typically 300 mm long with a diameter of 50 mm. Along part of its length the rod remains separated from adjacent regions by connective tissue papillae, which gives it a degree of independent mobility. The push rod is hypothesized to play a role in signaling contact with prey, particularly in moist or aquatic environments where electroreception is advantageous. A functionally similar structure, termed a domed pressure receptor (DPR), has been reported on the rostrum of the American alligator, Alligator mississippiensis. The DPR is hypothesized to play a role in detecting the disturbance of water by prey. The types of receptors present at the base of the DPR await elucidation, but it is likely that paciniform corpuscles are present. The avian homolog of the Pacinian corpuscle is the Herbst corpuscle, which is present in the skin of the bill of wading and aquatic birds and in other species, and also in other bodily locations, including the legs and trunk. Herbst corpuscles are

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particularly dense in the bill tip organ of the goose and duck, and general agreement exists that they function as RA receptors with frequency-following characteristics similar to Pacinian corpuscles.
Ruffini Corpuscle

favored, in turn, a greater degree of cortical investment devoted to the interpretation of those sensory inputs.
See also: Electrical Perception and Communication; Enteric Nervous System: Sensory Pathways; Seismic and Vibrational Signals in Animals; Sensory System Specializations; Tactile Texture.

Angelo Ruffini (18641929) reported cigarlike structures in 1893. Ruffini corpuscles consist of a long fusiform, encapsulated structure innervated by a myelinated large-caliber (612 mm) axon terminating as numerous branches intertwined among collagen bundles. Ruffini corpuscles have been reported in glabrous and hirsute skin, as well as in the tendinous insertions and joint capsules of mammals. Because of their regular discharge property in cats, they are classified as SA type II mechanoreceptors in contrast to the irregular discharge properties of SA type I fibers. Ruffini corpuscles are sensitive to skin stretch, particularly tangential forces generated in the skin during tasks like grasping.

Further Reading
Castano P, Ventura RG, and Maddalone M (1985) Notes on morpho-functional differences between Meissners corpuscle of man and the green monkey (Cercopithecus aethiops L). Folia Morphologica 33: 294298. Catania KC and Remple FE (2004) Tactile foveation in the starnosed mole. Brain, Behavior, and Evolution 63: 112. Fagan BM and Cahusac PM (2001) Evidence for glutamate receptor mediated transmission at mechanoreceptors in the skin. Neuroreport 12: 341347. Granovsky Y, Matre D, Sokolik A, Lorenz J, and Casey KL (2005) Thermoreceptive innervation of human glabrous skin: A contact heat evoked potential analysis. Pain 115: 238247. Hoffman JN, Montag AG, and Dominy NJ (2004) Meissner corpuscles and somatosensory acuity: The prehensile appendages of primates and elephants. Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 281: 11381147. Iggo A and Andres KH (1982) Morphology of cutaneous receptors. Annual Review of Neuroscience 5: 131. Lumpkin EA and Caterina MJ (2007) Mechanisms of sensory transduction in the skin. Nature 445: 858865. Pare M, Elde R, Mazurkiiewicz JE, Smith AM, and Rice FL (2001) The Meissner corpuscle revised: A multiafferented mechanoreceptor with nociceptor immunochemical properties. Journal of Neuroscience 21: 72367246. Pettigrew JD, Manger PR, and Fine SLB (1998) The sensory world of the platypus. Proceedings of the Royal Society of London Series B 353: 11991210. Proske U, Gregory JE, and Iggo A (1998) Sensory receptors in monotremes. Proceedings of the Royal Society of London Series B 353: 11871198. Soares D (2002) An ancient sensory organ in crocodilians. Nature 417: 241242. Takahashi-Iwanaga H and Shimoda H (2003) The three-dimensional microanatomy of Meissner corpuscles in monkey palmar skin. Journal of Neurocytology 32: 363371.

Evolution of Cutaneous Receptors

In general, the morphological principles and mechanisms of cutaneous receptors are conserved across vertebrate orders. Each type of receptor responds to specific stimuli and contributes to the global perception of texture in the central nervous system. Specialized nerve endings of the glabrous skin tend to vary in density according to the particular locomotor or foraging behavior of an animal species. For instance, Meissner corpuscles are more complex and densely packed in the digits of primates than in other mammals, which lack the same degree of forelimb opposability. Species with very specialized receptor structures, such as the star-nosed mole and platypus, tend to also have a highly developed somatosensory cortex. The evolution of specialized receptors in the glabrous skin thus appears to result primarily from selection for the reorganization and concentration of preexisting cells. Improved somatosensory acuity