Low-Threshold Mechanosensory

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.

Receptive Field Properties

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.

Dorsal Column—Medial Lemniscus Pathway

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.

The third-order neurons of the pathway are located in the ventral posterior lateral (VPL) nucleus of the thalamus and project to somatosensory areas of the cerebral cortex (Fig. 7-5).

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.