Cutaneous receptors

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The sense of touch is tied to the skin, the most accessible and largest organ in our body. Skin contains a multitude of highly diverse receptors that underlie our sense of touch, pressure, vibration, pain, and temperature. Neural circuits involved in processing information relating to discriminative touch needed for recognizing and manipulating objects, are distinct from circuits that process information pertaining to pain and temperature, which are distinct from circuits that process information about social (affective, pleasant) touch. Large diameter myelinated fibers signal touch-pressure and body position, and transmit this information via the dorsal column-medial lemniscal system to the primary somatosensory cortex. Smaller diameter fibers signal pain and temperature and project via the spinothalamic system to the primary somatosensory cortex. Unmyelinated C tactile fibers signal pleasantness of touch, and they project via the spinothalamic system to the secondary somatosensory (posterior insular) cortex.

Mechanoreceptors are by definition receptors located in the skin, the muscles, tendons, joints, and deep tissues that transduce mechanical energy associated with specific aspects of touch-pressure applied to the skin into neural signals. Mechanoreceptors vary both in receptive field size and in their rate of adaptation. Five basic types of mechanoreceptors are found in the skin and in subcutaneous layers of fatty and connective tissue. Four types of mechanoreceptors (Merkel disc, Meissner’s corpuscle, Ruffini ending, and Pacinian corpuscle) are found in the glabrous (hairless) skin of the hands, soles of the feet, and the lips. One type (hair follicle receptor) is found exclusively in hairy skin.

Merkel disc

Merkel discs are located deep in the epidermis at the peaks of the primary epidermal ridges. Merkel discs are present at very high densities in the skin of the fingertips and lips and at very low density in hairy skin. They are exquisitely sensitive to small forces that produce skin indentations as little as 50 m. Electrical recordings of single fibers that innervate Merkel discs indicate that they are slowly adapting receptors, i.e. they continue to fire action potentials for as long as the indentation continues.

Meissner corpuscle

Meissner’s corpuscles are located in the upper dermis, close to the border with the epidermis. They are present at extremely high densities in the skin of the fingertips; they are not found in hairy skin. Meissner corpuscles are exquisitely sensitive to skin indentation but their ability to localize these movements is modest because a single sensory afferent fiber branches and innervates a group of Meissner corpuscles. This pattern of innervation results in a receptive field characterized by multiple points of high sensitivity, each marking the position of a Meissner corpuscle innervated by the fiber (Fig. 23-4C). Meissner corpuscles are fast adapting receptors, i.e. they respond only at the onset and offset of prolonged skin indentation.

When we grip and lift objects, tiny movements (micro-slips) occur between our skin and the object. Meissner’s corpuscles detect these micro-slips. Signals transmitted to spinal circuits by the primary sensory afferents that innervate Meissner’s corpuscles serve to precisely and reflexively, i.e. without having to think about it, adjust the force of contraction of the relevant finger muscles in order to eliminate the micro-slips. The overall result is that when we grip and lift objects, we do so with the minimal grip force required. The importance of being able to automatically fine-tune grip strength becomes readily apparent when picking ripe raspberries or when lifting an egg.

Ruffini ending

Ruffini endings are located deep in the dermis at relatively low densities. Their longitudinal axis is orientated parallel to the skin surface, which may explain why they are highly sensitive to horizontal skin stretch but relatively insensitive to skin indentation. Ruffini endings are slowly adapting and respond to the amplitude of skin stretch rather than the rate at which it is stretching. Responses are selective for the direction of skin stretch – they may be sensitive for stretch in one direction and be unresponsive for a stretch in the opposite direction as is illustrated by the direction of arrows for the receptive fields on the middle and ring finger in Fig. 23-4. Ruffini endings may serve to provide information about hand and finger position, which is important for controlling digit movements.

Pacinian corpuscle

Pacinian corpuscles are located deep within the dermal layer of skin. Their density is relatively modest: there are about 350 Pacinian corpuscles per finger. Like Meissner’s corpuscles, they are fast adapting receptors, i.e. they only respond at the onset and offset of skin indentation. The receptive field of a Pacinian corpuscle has a single point of maximal sensitivity that overlies the Pacinian corpuscle (Fig. 23-4C). Pacinian corpuscles are exquisitely sensitive to vibration but are poor at localization. They are most sensitive to relatively high-frequency vibration (200-300 Hz). Within this range of frequencies, they can detect skin indentations as small as 10 nm. In addition to detecting skin indentation, Pacinian corpuscles play a role at detecting transient and vibratory stimuli transmitted to the hand by handheld objects like tools or probes.

Hair follicle (hairy skin)

Primary sensory afferent neurons that innervate the hair follicle receptor spiral around the base of the hair follicle or form a lattice-like pattern. Most hair follicle afferents are fast-adapting; they respond to bending of the hair and signal the direction and velocity of objects brushing against hairy skin; they do not respond to sustained deflection of the hair.

Converging evidence from electrophysiological recording, psychophysical studies on people with sensory neuronopathies, and functional brain imaging indicates that affective aspects of touch are signaled by low threshold mechanoreceptive C tactile (CT) afferents (Liljencrantz & Olausson, 2014; McGlone, Wessberg, & Olausson, 2014). C tactile fibers exclusively innervate hairy skin. Their endings wrap around hair follicles, which enable them to respond to deflection of the hairs. CT fibers innervate the small, so-called vellus hairs. Interestingly, vellus hairs are also innervated by Aβ and Aδ fibers. Thus, deflection of vellus hairs gives rise to multiple responses: a fast, emotionally neutral signal mediated by Aβ fibers, and a slow, diffuse signal that conveys pleasant touch mediated by C tactile fibers. Conduction velocities of CT fibers are slow: between 0.6 – 1.3 m/s. Single unit recording has shown that a slowly moving caress strongly activates CT afferents (Loken, Wessberg, Morrison, McGlone, & Olausson, 2009). The greatest firing rates are recorded with caresses that move at velocities in the range of 1-10 m/s (Fig. 3A), which is the same range of stimulus speeds that is associated with maximal sunjective pleasantness ratings in psychophysical studies (Fig. 3B). In fact, firing frequency of CT afferents predicts perceived pleasantness in response to soft brush stroking (Fig. 3C) (Liljencrantz & Olausson, 2014; Loken et al., 2009). Thus, C tactile afferents appear to be tuned to detect a specific type of touch: a light caress with a speed that is optimal for inducing a pleasant sensation.

Direct evidence for a role of C tactile afferents in pleasant touch has been difficult to come by because due to the fact that individual hair follicles are innervated by both Aβ and C tactile afferents, CT afferents cannot be activated without also activating Aβ fibers. Patients suffering from peripheral sensory neuronopathy, a rare disorder that selectively destroys the cell bodies of large primary sensory afferents (Sacks, 1985; Sterman Ab Fau – Schaumburg, Schaumburg Hh Fau – Asbury, & Asbury), lack large myelinated Aβ fibers but have intact C tactile fibers. Reexamination of the tactile sensibility of two well studied subjects with peripheral sensory neuronopathy (GL and IW) revealed that both subjects lacked fast, discriminative touch but retained the ability to detect diffuse pleasant touch (Olausson et al., 2008; Olausson et al., 2002). Importantly, the sense of pleasant touch was present in hairy skin but was never found in glabrous skin, indicating that the diffuse sensations were mediated by surviving C tactile afferents, which innervate hairy but not glabrous skin.

Brain imaging studies in healthy subjects have reported that light brush strokes on the forearm activate primary and secondary somatosensory cortices, which have been implicated in discriminative touch, in addition to the posterior insula, which is involved in emotional aspects of touch perception. Imaging brains of subjects with sensory neuronopathy revealed activation of the posterior insular cortex but not the primary and secondary somatosensory cortices, suggesting that the remaining C tactile afferents activate the posterior insula but not the primary and secondary somatosensory cortices (Olausson et al., 2002).

A genetic mutation in a select group of individuals that reside in Norrbotton, a region of Sweden, north of the artic circle, affects the production of a protein, nerve growth factor beta (NGFbeta), which is critical to the survival of small sensory neurons. People afflicted with the Norrbotton mutation (HSAN-V, hereditary sensory and autonomic neuropathy type V) present with a loss of C tactile fibers and Aδ fibers, and sparing of the larger Aα and Aβ fibers. Thus, carriers of the Norrbotton mutation have essentially the opposite fiber complement than patients with sensory neuronopathy. The Norrbotton population perceives gentle caresses as significantly less pleasant as control subjects, and brain scans indicate only a weak activation of the posterior insula (Morrison et al., 2011).

The combined results are consistent with the view that C tactile afferents innervate hairy skin and function as caress detectors that project to the posterior insula, activation of which makes a critical contribution to the perception of affective (pleasant) touch.

Musculoskeletal receptors

The musculoskeletal system contains five basic types of mechanoreceptors that belong to the large fiber system: muscle spindles in muscles, Golgi tendon organs in tendons, and Ruffini-like and Paciniform receptors, and Golgi endings in joints and ligaments.

Golgi tendon organs (GTOs)

In order to produce accurate movements the CNS needs information about the force of muscle contraction. GTOs provide such information. Information about muscle force is also necessary for maintaining a steady grip on an object and for compensation for muscle fatigue. GTOs are encapsulated structures approximately 1 mm long and 0.1 mm in diameter. They are located between muscle fibers and tendon; they are therefore arranged in series with skeletal muscle fibers. Each GTO is innervated by a single sensory axon, the so-called Ib afferent. Multiple unmyelinated endings of the Ib afferent intertwine with braided collagen fibers. When the GTO is stretched (usually because of contraction rather than lengthening of the muscle), the collagen fibers deform the sensory endings of the Ib afferent neuron, which increases its firing rate. Thus, the GTO is much more sensitive to active muscle contraction than passive muscle stretch. The mean firing rate of the population of GTOs in a given muscle is proportional to the force of muscle contraction, which is consistent with the view that GTOs continuously measure and provide information about the force of muscle contraction.

Muscle spindles

Muscle spindles are sensory receptors in muscles that signal changes in muscle length (stretch) and the rate at which muscle length changes (velocity of stretch). Because muscle length varies with the angle of the joint on which the muscle acts, the brain uses information about muscle length to determine relative positions of body segments.

Muscle spindles are encapsulates structures that are fusiform in shape, i.e. they are shaped in the form of a spindle. Muscle spindles are arranged in parallel with the muscle fibers that are involved in generating skeletal muscle force. They vary in length from approximately 2 to 10 mm, and they are distributed throughout the muscle belly of all skeletal muscles, with the exception of perioral muscles, which move the lips, and the muscles of the inner ear. Their density if particularly high in muscles of the neck and hands.

 

Muscle spindles consist of three components: intrafusal muscle fibers, afferent sensory endings, and efferent motor endings. Intrafusal (i.e. inside the spindle) muscle fibers are specialized muscle fibers with central regions that are non-contractile. Intrafusal muscle fibers do not contribute to the generation of muscle force; they are distinguished from extrafusal muscle fibers, which are the fibers that generate the main force of contraction. Intrafusal fibers differ in their contractile properties. There are two main types of intrafusal fibers: nuclear bag fibers and nuclear chain fibers (Fig. 35-3B).

Each intrafusal fiber is innervated by one or more sensory axons that wrap around the central part of the intrafusal fibers. The sensory afferents increase firing when the central region is stretched, and decrease firing upon release of stretch. Together, all terminations of a single group Ia afferent on intrafusal fibers make up a primary ending, and all terminations of a single group II afferent make up a secondary ending (Fig. 35-3B).

Efferent (motor) axons terminate on the two end regions of the intrafusal fibers. They change the sensitivity of the muscle spindle. These are axons of a special type of motor neurons, the γ-motoneurons, as opposed to the α-motor neurons that innervate the extrafusal muscle fibers and generate the muscle’s contractile force. Increased firing of γ-motoneurons contracts the two end regions of the intrafusal fibers, which stretches the central, length-monitoring region of the intrafusal fiber, thereby increasing the sensitivity of the spindle. We distinguish static and dynamic γ-motor neurons, depending on the specific types of intrafusal fibers innervated by the γ-motor neurons (Fig. 35-3B). Figure 35-3C illustrates the effect of stimulating γ-motor neurons on the discharge pattern of a Ia afferent. Activation of static γ-motor neurons during muscle stretch increases the steady state firing rates of Ia afferents relative to the firing rate without stimulation. During the stretch, the dynamic response is reduced. Stimulation of the dynamic γ-motor neuron results in a small increase in static response but a large increase in dynamic response. Thus, innervation of muscle spindles by independently controlled γ-motor neurons provides the brain with a mechanism to adjust the spindle’s sensitivity and thus fine-tune the information it receives.

When α-motor neurons (i.e. those that innervate extrafusal muscle fibers) contract and the muscle shortens, γ-motor neurons are activated simultaneously to prevent the intrafusal fibers from slackening. The simultaneous activation of α-motor neurons and γ-motor neurons is called α- γ coactivation. α- γ coactivation keeps the intrafusal fiber under tension and maintains the firing rate of the Ia fibers in a range that is optimal for signaling changes in muscle length, regardless of the actual length of the muscle. Thus, α-γ coactivation stabilizes the sensitivity of the muscle spindles — it is characteristic of many voluntary movements.

Joint receptors

Joint receptors are mechanoreceptors that are found in the ligaments and soft tissues of joints. They are of different types: Ruffini-like, Paciniform, and Golgi receptors. Joint receptors are innervated by afferent fibers of similar types as those that innervate cutaneous and muscle receptors, and they have similar adaptation characteristics. Deformation of the joint capsule activates Paciniform and Ruffini-like receptors; stretch of ligaments activates Golgi endings. Recording of joint receptor afferent fibers has demonstrated that the receptors are activated primarily at extreme joint positions, which is consistent with the view that joint receptors are limit detectors that protect joints from hyperextension.