CHAPTER 7 The Somatosensory System
The somatosensory system provides information to the central nervous system (CNS) about the state of the body and its contact with the world. It does so by using a variety of sensory receptors that transduce mechanical (pressure, stretch, and vibrations) and thermal energies into electrical signals. These electrical signals are called generator, or receptor, potentials and occur in the distal ends of axons of first-order somatosensory neurons, where they trigger action potential trains that reflect information about the characteristics of the stimulus. The cell bodies of these neurons are located in dorsal root (Fig. 7-1, A; see Fig. 4-8) and cranial nerve ganglia.
Figure 7-1 Ascending somatosensory pathways from the body. A, First-, second-, and third-order neurons are shown for the two main pathways conveying cutaneous information from the body to the cerebral cortex: the dorsal column/medial lemniscal and the spinothalamic pathways. Note that the axon of the second-order neuron crosses the midline in both cases, so sensory information from one side of the body is transmitted to the opposite side of the brain, but the levels in the neuraxis at which this takes place are distinct for each pathway. Homologous central pathways for the head originate in the trigeminal nucleus and are described in text, but they are not illustrated for clarity. B, Major spinocerebellar pathways carrying tactile and proprioceptive information to the cerebellum from the upper and lower parts of the body. Again, pathways from the head originate in the trigeminal nuclei but are not shown for clarity. A midsagittal view of the nervous system shows the levels of the spinal and brainstem cross sections in panels A and B.
Each ganglion cell gives off an axon that after a short distance, divides into a peripheral process and a central process. The peripheral processes of the ganglion cells coalesce to form peripheral nerves. A purely sensory nerve will have only axons from such ganglion cells; however, mixed nerves, which innervate muscles, will contain both afferent (sensory) fibers and efferent (motor) fibers. At the target organ, the peripheral process of an afferent axon divides repeatedly, with each terminal branch ending as a sensory receptor. In most cases, the free nerve ending by itself forms a functional receptor, but in some, the nerve ending is encapsulated by accessory cells, and the entire structure (axon terminal plus accessory cells) forms the receptor.
The central axonal process of the ganglion cell either enters the spinal cord via a dorsal root or enters the brainstem via a cranial nerve. A central process typically gives rise to numerous branches that may synapse with a variety of cell types, including second-order neurons of the somatosensory pathways. The terminal location of these central branches varies depending on the type of information being transmitted. Some terminate at or near the segmental level of entry, whereas others project to brainstem nuclei.
Second-order neurons that are part of the pathway for the perception of somatosensory information project to specific thalamic nuclei, where the third-order neurons reside. These neurons in turn project to the primary somatosensory cortex (S-I). Within the cortex, somatosensory information is processed in S-I and in numerous higher-order cortical areas. Somatosensory information is also transmitted by other second-order neurons to the cerebellum for use in its motor coordination function.
The organization of the somatosensory system is quite distinct from that of the other senses, which has both experimental and clinical implications. In particular, other sensory systems have their receptors localized to a single organ, where they are present at high density (e.g., the eye for the visual system). In contrast, somatosensory receptors are distributed throughout the body (and head). In addition, the other senses convey their information to the brain via a single nerve bundle (or in one case, via two to three nerves), whereas somatosensory information arrives via spinal dorsal roots and cranial nerves (primarily the trigeminal).
The somatosensory system receives three broad categories of information based on the distribution of its receptors. Its exteroceptive division is responsible for providing information about contact of the skin with objects in the external world, and a variety of cutaneous mechanoceptive, nociceptive (pain), and thermal receptors are used for this purpose. Understanding this division will be the main focus of this chapter. The proprioceptive component provides information about body and limb position and movement and relies primarily on receptors found in the joints, muscles, and tendons. Because these receptors initiate pathways that in part are intimately involved in the control of movement, they will be discussed in Chapter 9; however, the ascending central pathways that originate with them and that underlie conscious and unconscious proprioceptive functions will be covered later in this chapter. Finally, the enteroceptive division has receptors for monitoring the internal state of the body and includes mechanoreceptors that detect distention of the gut or fullness of the bladder.
The somatosensory pathways can also be classified by the type of information that they carry. Two broad functional categories are recognized, each of which subsumes several somatosensory submodalities. Fine discriminatory touch sensations include light touch, pressure, vibration, flutter (low-frequency vibration), and stretch or tension. The second major functional group of sensations is that of pain and temperature. Submodalities here include both noxious and innocuous cold and warm sensations and mechanical and chemical pain. Itch is also closely related to pain and appears to be carried by particular fibers associated with the pain system.
The sensory functions of various cutaneous sensory receptors have been studied in human subjects with a technique known as microneurography, in which a fine metal microelectrode is inserted into a nerve trunk in the arm or leg to record the action potentials from single sensory axons. When a recording can be made from a single sensory axon, the receptive field of the fiber is mapped. Most of the various types of sensory receptors that have been studied in experimental animals have also been found in humans with this technique.
After the receptive field of a sensory axon has been characterized, the electrode can be used to stimulate the same sensory axon. In these experiments the subject is asked to locate the perceived receptive field of the sensory axon, which turns out to be identical to the mapped receptive field.
Of great importance experimentally, the afferent fibers that convey these somatosensory submodalities to the CNS are different sizes. Recall that the compound action potential recorded from a peripheral nerve (Table 5-1) consists of a series of peaks, thus implying that the diameters of axons in a nerve are grouped rather than being uniformly distributed. Information about tactile sensations is carried primarily by large-diameter myelinated fibers in the Aα and Aβ classes, whereas pain and temperature information travels via small-diameter, lightly myelinated (Aδ) and unmyelinated (C) fibers. It is possible to block or selectively stimulate a class of axons of particular size, thereby allowing study of the different somatosensory submodalities in isolation.
The skin is an important sensory organ and, not surprisingly, is richly innervated with a variety of afferents. We first consider the afferent types related to fine or discriminatory touch sensations. These afferents are related to what are called low-threshold mechanoreceptors. Nociceptor and thermoceptor innervation will be considered separately in a later section of this chapter.
To study the responsiveness of tactile receptors, a small-diameter rod or wire is used to press on a localized region of skin. With this technique, two basic types of responses may be seen when recording sensory afferent fibers: fast-adapting (FA) and slow-adapting (SA) responses (Fig. 7-2). They are present in similar quantities. FA fibers will show a short burst of action potentials when the rod first pushes down on the skin, but then they will cease firing despite continued application of the rod. They may also burst at the cessation of the stimulus (i.e., when the rod is lifted off). In contrast, SA units will start firing action potentials (or increase their firing rate) at the onset of the stimulus and continue to fire until the stimulus ends (Fig. 7-2).
Figure 7-2 Cutaneous mechanoreceptors and the response patterns of associated afferent fibers. A, Schematic views of glabrous (hairless) and hairy skin showing the arrangement of the various major mechanoreceptors. B, Firing patterns of the different cutaneous low-threshold mechanosensitive afferent fibers that innervate the various encapsulated receptors of the skin.
(Traces in B are based on data from Johansson RS, Vallbo ÅB: Trends Neurosci 6:27, 1983.)
Both the FA and SA afferent classes can be subdivided on the basis of other aspects of their receptive fields, where receptive field is defined as the region of skin from which stimuli can evoke a response (i.e., change the firing of the afferent axon). Type 1 units have small receptive fields with well-defined borders. Particularly for glabrous skin (i.e., hairless skin, such as on the palms of the hands and soles of the feet), the receptive field has a circular or ovoid shape, within which there is relatively uniform and high sensitivity to stimuli that decreases sharply at the border (Fig. 7-3). Type 1 units, particularly SA1 units, respond best to edges. That is, a larger response is elicited from them when the edge of a stimulus cuts through their receptive field than when the entire receptive field is indented by the stimulus.
Figure 7-3 Receptive field characteristics for type 1 and type 2 sensory afferents. Plots in the top row show the threshold level of force needed to evoke a response as a function of the distance across the receptive field. Receptive field size is shown on the hand below each plot.
(Data from Johansson RS, Vallbo ÅB: Trends Neurosci 6:27, 1983.)
Type 2 units have wider receptive fields with poorly defined borders and only a single point of maximal sensitivity, from which there is a gradual reduction in sensitivity with distance (Fig. 7-3). For comparison, a type 1 unit’s receptive field typically will cover approximately four papillary ridges in the fingertip, whereas a type 2 unit will have a receptive field that covers most or all of a finger.
Thus, four main classes of low-threshold mechanosensitive afferents have been identified physiologically (FA1, FA2, SA1, and SA2). Peripherally, these axons may terminate as either free nerve endings or within a capsule made up of supporting cells.
For glabrous skin, the four afferent classes have been associated with four specific types of histologically identified receptor capsules whose locations and physical structure help explain the firing properties of these sensory afferents. FA1 afferents terminate in Meissner’s corpuscles, whereas SA1 afferents terminate in Merkel’s disks. In both cases the capsule is located relatively superficially, either in the basal epidermis (Merkel) or just below the epidermis (Meissner) (Fig. 7-2). These capsules are small and oriented to detect stimuli pressing down on the skin surface just above them, thus allowing SA1 and FA1 afferents to have small receptive fields. For glabrous skin, SA2 afferents terminate in Ruffini’s endings and FA2 afferents end in Pacinian corpuscles. Both these receptors lie deeper in the dermis and connective tissue and therefore are sensitive to stimuli applied over much larger territory. Both Pacinian and Meissner’s capsules act to filter out slowly changing or steady stimuli, thus making these afferents selectively sensitive to changing stimuli.
For hairy skin, the relationship between receptors and afferent classes is similar to that of glabrous skin. SA1 and SA2 fibers connect to Merkel’s and Ruffini’s endings, the same as for glabrous skin. Pacinian corpuscles also underlie the properties of FA2 afferents; however, they are not found in hairy skin but, instead, are located in deep tissues surrounding muscles and blood vessels. There is not an exact analogue to the FA1 afferents. Rather, there are hair units, which are afferents whose free endings wrap around hair follicles (Fig. 7-2). Each such hair unit will connect with about 20 hairs to produce a large ovoid or irregularly shaped receptive field. These units are extremely sensitive to movement of even a single hair. There are also field units that respond to touch of the skin, but unlike FA1 units, they have large receptive fields.
Several psychophysical and neural coding questions can be related to the receptive field properties and sensitivities of the various categories of afferents. For example, is the threshold of perception of tactile stimuli due to the sensitivity of the peripheral receptors or to central processes? In fact, by using microneurography, it is possible to show that a single spike in an FA1 afferent from the finger can be perceived, thus indicating that the receptors limit the sensitivity; however, for other skin regions, perception is more dependent on central factors such as attention.
An important behavioral and clinical measure of somatosensory function is spatial acuity or two-point discrimination. Clinically, a doctor will apply two needle-like points simultaneously to the skin of a patient. The patient will generally perceive the points as two distinct stimuli as long as they are farther apart than some threshold distance, which varies across the body. The best discrimination (shortest threshold distance) is at the fingertips. Type 1 units underlie spatial acuity, which is not surprising given the smaller receptive fields of type 1 units than type 2 units; moreover, the threshold distance for a region of skin is most closely related to its density of type 1 units because these units have similarly sized receptive fields throughout the glabrous skin but their density falls off from fingertip to palm to forearm and this fall-off correlates with the rise in threshold distance. Note that this variation in innervation density also matches the overall sensitivity of different skin regions to cutaneous stimuli.
The relationship of the firing rates in the various afferent classes to perceived stimulus quality is another important issue that has been addressed with microneurographic techniques. When a single SA fiber is stimulated with brief current pulses such that each pulse triggers a spike, a sensation of steady pressure is felt at the receptive field area of that fiber. As pulse frequency is intensified, an increase in pressure is perceived. Thus, the firing rate in SA fibers codes for the force of the tactile stimulus. As another example, when an FA fiber is repetitively stimulated, a sensation of tapping results first, and as the frequency of the stimulus is increased, the sensation turns to one of vibration. Interestingly, in neither case does the stimulus change its qualitative character, for example, to a feeling of pain, as long as the stimulus activates only a particular fiber class. This is evidence that pain is a distinct submodality that uses a set of fibers distinct from those used by low-threshold mechanoreceptors.
These findings illustrate an important principle of sensory systems called labeled line. The idea is that the quality (i.e., modality) of a particular sensation results from the fact that it is conveyed to the CNS by a specific set of afferents that have a distinct set of targets in the nervous system. Alterations in activity in these afferents will therefore change only quantitative aspects of the sensation. As will be seen in more detail later, the various somatosensory submodalities (i.e., information arising from FA and SA mechanoreceptors, proprioceptors, and nociceptors) appear to use relatively separate dedicated cell populations, even at relatively high levels of the CNS, such as the thalamus and primary somatosensory cortex.
Axons of the peripheral nervous system (PNS) enter or leave the CNS through the spinal roots (or through cranial nerves). The dorsal root on one side of a given spinal segment is composed entirely of the central processes of dorsal root ganglion cells. The ventral root consists chiefly of motor axons, including α motor axons, γ motor axons (see Chapter 9), and at certain segmental levels, autonomic preganglionic axons (see Chapter 11).
The pattern of innervation is determined during embryological development. In adults, a given dorsal root ganglion supplies a specific cutaneous region, which is called a dermatome. Many dermatomes become distorted during development, chiefly because of rotation of the upper and lower extremities as they are formed, but also because humans maintain an upright posture. However, the sequence of dermatomes can readily be understood if depicted on the body of a person in a quadrupedal position (Fig. 7-4).
Figure 7-4 A, Dermatomes represented on a drawing of a person assuming a quadrupedal position. B, Sagittal view of the spinal cord showing the origin of nerves corresponding to each of the dermatomes shown in A.
Although a dermatome receives its densest innervation from the corresponding spinal cord segment, collaterals of afferent fibers from the adjacent spinal segments also supply the dermatome. Thus, transection of a single dorsal root causes little sensory loss in the corresponding dermatome. Anesthesia of any given dermatome requires the interruption of several adjacent dorsal roots.
Within the dorsal roots, fibers are not randomly distributed. Rather, the large myelinated primary afferent fibers assume a medial position in the dorsal root, whereas the fine myelinated and unmyelinated fibers are more lateral. The large, medially placed afferent fibers enter the dorsal column, where they bifurcate to form rostrally and caudally directed branches. These branches give off collaterals that terminate in the several neighboring segments. The rostral branch also ascends to the medulla as part of the dorsal column—medial lemniscus pathway. The axonal branches that terminate locally in the spinal cord gray matter transmit sensory information to neurons in the dorsal horn and also provide the afferent limb of reflex pathways (see Chapter 9).
A common disease that illustrates the dermatomal organization of the dorsal roots is shingles. Shingles is the result of reactivation of the herpes zoster virus, which typically causes chickenpox during the initial infection. During the initial infection the virus infects dorsal root ganglion cells, where it can remain latent for years to decades. When the virus reactivates, the cells of that particular dorsal root ganglion become infected, and the virus travels along the peripheral axon branches and gives rise to a painful or itchy rash that is confined to one side of the body (ends at the midline) in a dermatomal or belt-like distribution.
The trigeminal nuclear complex consists of four main divisions, three of which are sensory. The three sensory divisions (from rostral to caudal) are the mesencephalic, chief (or main) sensory, and spinal (or descending) trigeminal nuclei. The latter two are typical sensory nuclei in that the cell bodies contained in them are second-order neurons. The mesencephalic nucleus actually contains first-order neurons and thus is analogous to a dorsal root ganglion. The last division of the trigeminal complex is the motor nucleus of the trigeminal nerve, whose motor neurons project to skeletal muscles of the head via the trigeminal nerve (see Fig. 4-7, C-G).
The arrangement of primary afferent fibers that supply the face is comparable to that of fibers that supply the body and is provided for primarily by fibers of the trigeminal nerve. Peripheral processes of neurons in the trigeminal ganglion pass through the ophthalmic, maxillary, and mandibular divisions of the trigeminal nerve to innervate dermatome-like regions of the face. These fibers carry both tactile information and pain and temperature information. The trigeminal nerve also innervates the teeth, the oral and nasal cavities, and the cranial dura mater.
The central processes of trigeminal ganglion cells enter the brainstem at the midpontine level, which also corresponds to the level of the chief sensory trigeminal nucleus (nucleus of cranial nerve V). Some axons terminate in this nucleus (primarily large-caliber axons carrying the information needed for fine discriminative touch), whereas others (intermediate- and small-caliber axons that carry information about touch, as well as pain and temperature) form the spinal trigeminal tract, which descends through the medulla just lateral to the spinal trigeminal nucleus. As the tract descends, axons peel off and synapse in the nucleus.
Proprioceptive information is also conveyed via the trigeminal nerve; however, in this unique case, the cell bodies of the first-order fibers are located within the CNS in the mesencephalic portion of the trigeminal nucleus. The central processes of these neurons terminate in the motor trigeminal nucleus (to subserve segmental reflexes equivalent to the segmental spinal cord reflexes—see Chapter 9), the reticular formation, and the chief sensory trigeminal nucleus.
As may already be clear, information related to the different somatosensory submodalities travels, to a large extent, via separate pathways up the spinal cord and brainstem. For example, from the body, fine discriminatory touch information is conveyed by the dorsal column—medial lemniscus pathway, whereas pain, temperature, and crude touch information is conveyed by the anterolateral system.
Proprioceptive information is transmitted by yet another route that partially overlaps with the dorsal column—medial lemniscal pathway. Note, however, that this functional segregation is not absolute, so, for example, there can be some recovery of discriminative touch ability after a lesion of the dorsal columns. The anterolateral system will be discussed in the section on pain because it is the critical pathway for that information. Here, the central pathways for discriminatory touch and proprioception are considered in detail.
This pathway is shown in its entirety in Figure 7-1, A. The dorsal columns are formed by ascending branches of the large myelinated axons of dorsal root ganglion cells (the first-order neurons). These axons enter at each spinal segmental level and travel rostrally up to the caudal medulla to synapse in one of the dorsal column nuclei: the nucleus gracilis, which receives information from the lower part of the body and leg, and the nucleus cuneatus, which receives information from the upper part of the body and arm. Note that in the dorsal columns and across the dorsal column nuclei there is a somatotopic representation of the body, with the legs represented most medially, followed by the trunk and then the upper limb. This somatotopy is a consequence of newly entering afferents being added to the lateral border of the dorsal funiculus as the spinal cord is ascended. Such somatotopic maps are present at all levels in the somatosensory system, at least through the primary sensory cortices.
The dorsal column nuclei are located in the medulla and contain the second-order neurons of the pathway for discriminatory touch sensation. These cells respond similarly to the primary afferent fibers that synapse on them (see the earlier description of afferent types). The main differences between the responses of dorsal column neurons and primary afferent neurons are as follows: (1) dorsal column neurons have larger receptive fields because multiple primary afferent fibers synapse on a given dorsal column neuron, (2) dorsal column neurons sometimes respond to more than one class of sensory receptor because of the convergence of several different types of primary afferent fibers on the second-order neurons, and (3) dorsal column neurons often have inhibitory receptive fields that are mediated through local interneurons.
The axons of dorsal column nuclear projection neurons exit the nuclei and are referred to as the internal arcuate fibers as they sweep ventrally and then medially to cross the midline at the same medullary level as the nuclei (Fig. 4-7, F). Immediately after crossing the midline, these fibers form the medial lemniscus, which projects rostrally to the thalamus. Knowledge of this decussation level is clinically important because damage to the dorsal column—medial lemniscal pathway below this level, which includes all of the spinal cord, will produce loss of fine somatosensory discriminatory abilities on the same, or ipsilateral, side of the lesion, whereas lesions above this level will produce contralateral deficits. Moreover, because there is a clear somatotopic arrangement of fibers in the medial lemniscus, localized lesions cause selective loss of fine-touch sensations limited to specific body regions.
Figure 7-5 Diagram of connections from the somatosensory receiving nuclei of the thalamus to the somatosensory cortex of the parietal lobe. Note the parallel flow of different types of somatosensory information through the thalamus and onto the cortex. CS, central sulcus; S1 and S2 are primary and secondary somatosensory areas, respectively. Note: collectively areas 3a, 3b, 1, and 2 are referred to as S1.