Many Sensory Receptors Have a Receptive Field, Allowing Them to Encode the Location of a Stimulus

Specific wiring patterns in ascending sensory pathways and in the cerebral cortex preserve information about the nature of a stimulus. In some sensory systems, individual receptors convey information not only about the nature of a stimulus but also about its location. That is, in addition to adequate stimuli, individual receptors may have receptive fields, particular areas in the periphery where application of an adequate stimulus causes them to respond. The receptive field of a cutaneous receptor, for example, is an area of skin where its receptive endings reside (Fig. 9-1). The receptive field of a retinal photoreceptor is some small location in the outside world whose image falls on the particular spot on the retina where that photoreceptor is located. This preservation of spatial information is apparent in the CNS as the common occurrence of distorted maps (see Fig. 3-30). Even arrays of receptors with no obvious spatial domain to map may have systematic representations of some other parameter, such as the mapping of sound frequencies in the cochlea and in auditory cortex (see Fig. 14-19).

Figure 9-1 Receptive fields of two cutaneous receptors.

Neurons in successive levels of sensory pathways—second-order neurons, thalamic and cortical neurons—also have receptive fields, although they may be considerably more elaborate than those of the receptors. Neurons in visual cortex, for example, typically respond not to spots of light but rather to edges with particular orientations.

Most Sensory Receptors Adapt to Maintained Stimuli, Some More Rapidly Than Others

Nearly all receptors show some adaptation, which means they become less sensitive during the course of a maintained stimulus. ^* Those that adapt relatively little are called slowly adapting and are suitable receptors for such things as static position. Those that adapt a great deal typically do so quickly and are called rapidly adapting; they are better suited to indicate change and movement of stimuli (Fig. 9-3). Some rapidly adapting receptors (e.g., the Pacinian corpuscles shown in Fig. 9-8) do so completely and signal only the beginning and end of a stimulus; others continue to respond, but at a diminished level, throughout a stimulus. Adaptation is usually a property of one or more parts of the receptor’s membrane: Ca ²⁺ ions entering through transduction channels, for example, set in motion biochemical processes that decrease the sensitivity of some receptors. In addition, various accessory structures may modify the physical stimulus before it reaches the sensory ending, as in the case of the multilayered capsules of Pacinian corpuscles.

Figure 9-3 Slowly adapting versus rapidly adapting receptors. In both, a receptor potential is produced in the sensory ending and spreads to a trigger zone, initiating action potentials that spread passively back into the sensory ending. A, A muscle spindle continues to fire action potentials as long as the muscle is stretched. B, Most hair receptors fire a short burst of action potentials and are then silent, even if the bending of the hair is maintained.

Figure 9-8 Some of the sensory endings found in glabrous skin. A, Schematic overview. M, Meissner corpuscle; Me, Merkel cell; PC, Pacinian corpuscle; R, Ruffini ending. B, Light micrograph of two Pacinian corpuscles from monkey skin, sectioned transversely. Multiple thin layers of each capsule surround a central mechanosensitive ending (arrows). C, Section of biopsied skin from a human fingertip, stained to show epidermis (blue fluorescence), myelin (red fluorescence), and nerve fibers (green fluorescence). Myelinated and unmyelinated axons course horizontally in a dermal plexus (thick arrows), giving off branches that end in Meissner corpuscles (thin arrows) and as Merkel endings (arrowheads). D, Higher-magnification view of a human Meissner corpuscle (actual size about 30 × 80 μm), stained as in C. A myelinated axon (thick arrow) enters the corpuscle, loses its myelin, and winds back and forth (thin arrows) between the stacked Schwann cells. Other unmyelinated fibers (arrowhead) head off into the epidermis to form free nerve endings.

(B, courtesy Dr. Nathaniel T. McMullen, University of Arizona College of Medicine. C and D, courtesy Dr. Maria Nolano, Salvatore Maugeri Foundation, Terme, Italy.)

Adaptation is a receptor-level process, but the CNS also has ways to regulate the sensitivity of receptors on a moment-to-moment basis. One such mechanism is the control of other structures related to receptors—for example, controlling the amount of light reaching the retina by regulating pupil size, or controlling the muscle fibers in stretch receptors (see Fig. 9-15). Another mechanism used is efferent projections from the CNS that synapse on receptor cells themselves; these are prominent in the inner ear (see Chapter 14) but occur in some other sensory systems as well.

Figure 9-15 Mechanism of action of gamma motor neurons. Muscle spindles in a contracted muscle (in this case, the biceps) are unstretched and thus electrically silent (A). As a result, slight stretching of the muscle causes little or no response (B). Activity of gamma motor neurons “prestretches” the central receptive region of the muscle spindle, causing some background activity when the biceps is contracted (C) and many more action potentials when it is stretched (D).

Sensory Receptors Use Ionotropic and Metabotropic Mechanisms to Produce Receptor Potentials

Sensory receptors transduce (Latin for “lead across”) some physical stimulus into an electrical signal—a receptor potential—that the nervous system can understand. Receptor potentials, like other electrical signals across neuronal membranes, are produced by the opening or closing of ion channels. (The only known exception in primates is the taste receptors that detect saltiness, as discussed in Chapter 13.) In many ways, most sensory receptors can be thought of as analogous to postsynaptic membranes, and their adequate stimuli as analogous to neurotransmitters (Fig. 9-5). Just as postsynaptic membranes use ionotropic and metabotropic mechanisms to produce postsynaptic potentials, almost all known transduction mechanisms involve ion channels whose conductance is affected either directly by a stimulus (as in transmitter-gated ion channels) or indirectly by way of a G protein–coupled mechanism. As in the case of synapses, some sensory receptors (e.g., somatosensory mechanoreceptors) produce depolarizing receptor potentials when stimulated, and others (e.g., photoreceptors) produce hyperpolarizing receptor potentials. Auditory and vestibular receptors can produce either, depending on the details of the stimulus.

Figure 9-5 Similarities between the general mechanisms of postsynaptic potentials and receptor potentials; a vestibular receptor cell (see Chapter 14) and an olfactory receptor cell (see Chapter 13) are used as examples, but almost all receptors use mechanisms that are similar in principle. A, Rapid synaptic transmission involves ligand-gated (ionotropic) channels (1) that bind neurotransmitter (2) and then change permeability (3). B, Cochlear and vestibular hair cells have channels that are anchored to the cytoskeleton and to one another. When there is little tension (1) in the filamentous proteins interconnecting the channels, they spend much of their time closed (2). Increasing the tension (3) by deflecting the microvilli bearing the channels causes direct opening of the channels (4) and depolarizing current flow. C, Slow synaptic transmission involves G protein–coupled (metabotropic) receptors (1). Dissociation of the G protein in response to neurotransmitter binding may affect ion channels either directly (2) or indirectly via enzymatic cascades (3). D, Olfactory receptor cells contain normally closed channels (1) and G protein–coupled receptors for odorants (2). Dissociation of the G protein activates an enzyme (3, adenylate cyclase), which catalyzes the production of a second messenger (cyclic AMP) that in turn opens the transduction channels (4), causing a depolarizing receptor potential.

Receptors with directly gated ion channels include the somatosensory receptors discussed in this chapter, auditory and vestibular receptors, some taste receptors, and some visceral receptors. Some have channels that are directly sensitive to mechanical distortion, and others have channels directly gated by some molecule or ion or by temperature changes. Receptors with a G protein–coupled transduction mechanism include photoreceptors, olfactory receptors, some taste receptors, and some visceral receptors.

All Sensory Receptors Produce Receptor Potentials, but Some Do Not Produce Action Potentials

Receptor potentials, like postsynaptic potentials, are focally produced events that spread electrotonically. If a particular sensory receptor is physically small relative to its length constant—that is, if it contacts the next cell in its neuronal pathway close to the site of transduction—the receptor potential itself can adequately modulate the rate of transmitter release at the synaptic terminal. This in turn causes a postsynaptic potential, and typically a change in action potential frequency, in the second cell (Fig. 9-6A). This is the case for many receptors, prominently including photoreceptors and auditory and vestibular receptors, all of which produce receptor potentials but no action potentials. Some receptors, however, must convey information over long distances (e.g., from a big toe to the spinal cord), even though the receptor potential dies out within a few millimeters. In such cases, most of the receptor, beginning near the site of transduction, is capable of propagating action potentials. The action potential frequency is then modulated by the receptor potential (Fig. 9-6B). Receptor potentials that directly cause changes in action potential frequency are also called generator potentials. All somatosensory receptors of the body operate in this manner, as do olfactory receptors and many visceral receptors. In vertebrates, all produce depolarizing receptor potentials, and an increased frequency of action potentials, in response to stimulation.

Figure 9-6 Short and long receptors, as illustrated by a hair cell of the inner ear (A) and a somatosensory ending (B). Hair cells produce a depolarizing receptor potential, but no action potentials, in response to deflection in the direction of the longest microvillar process (arrow). The receptor potential spreads passively to the synaptic area of the hair cell, where it increases the release of excitatory neurotransmitter (glutamate) onto the peripheral ending of an eighth nerve fiber. The postsynaptic potential then spreads passively to the trigger zone of the nerve fiber and initiates the firing of action potentials, which are conducted to synaptic terminals in the CNS. Events in the somatosensory receptor are similar, except that no peripheral synapse is involved: the trigger zone of the peripheral nerve fiber is part of the same neuron that contains the receptive ending.

Capsules and Accessory Structures Influence the Response Properties of Cutaneous Mechanoreceptors

In addition to mechanoreceptive free nerve endings, there are five other prominent types of mechanoreceptor found in the skin and adjacent subcutaneous tissue. Two are nonencapsulated endings with accessory structures, and three are encapsulated.

Endings around hairs vary in their degree of complexity. Those around the base of a cat’s whiskers are very elaborate, but those around most ordinary human body hairs are longitudinal neural processes or spiral endings that wrap around the base of the hair (Fig. 9-7). Bending the hair is presumed to deform the sensory ending, distort mechanically sensitive channels, and lead to the production of a generator potential. Most hair receptors are rapidly adapting; they respond well to something brushing across the skin but not to steady pressure. ^*

Figure 9-7 Two receptor types from hairy skin. Receptor endings wrap around hairs in a variety of configurations; a simple helical winding is shown. The inset is an enlarged drawing of a sensory nerve terminal (NT) forming a Merkel ending applied to a Merkel cell (M) in the basal layer of the epidermis. The Merkel cell is anchored among basal epidermal cells and has a prominent lobulated nucleus and dense-cored vesicles across from the sensory terminal.

The second type of nonencapsulated receptor is the Merkel ending, which is found in both hairy and glabrous skin (Fig. 9-7). The ending is a disk-shaped expansion of a terminal of a sensory fiber, which is applied to the base of a specialized cell called a Merkel cell. A single fiber branches to innervate several Merkel cells, which usually occur in clusters. Each Merkel cell is situated in the basal layer of the epidermis and contains dense-cored vesicles in what looks like a synaptic ending onto the sensory terminal. This apparent synapse naturally led to the hypothesis that the Merkel cell is sensitive to deformation and uses this synapse to pass information about mechanical stimuli along to the nerve ending (which would make it the only known example of a somatosensory receptor that is not part of a dorsal root ganglion cell). However, the available evidence is inconclusive, and the role of the Merkel cell is currently uncertain. Recordings from these sensory fibers have shown that Merkel endings are slowly adapting mechanoreceptors.

Meissner corpuscles are elongated, encapsulated endings in the dermal papillae of hairless skin just beneath the epidermis, oriented with their long axis perpendicular to the surface of the skin (Fig. 9-8). The encapsulation consists of a thin outer capsule and a layered stack of Schwann cells within the capsule, with the Schwann cells oriented perpendicular to the long axis of the capsule (like a stack of pancakes). One or more myelinated fibers approach the base of the corpuscle, lose their myelin, and wind back and forth between the stacked cells within the capsule. These are rapidly adapting receptors, and it is assumed that the capsule and the layered Schwann cells within it are important in determining the degree of adaptation. Vertical pressure on a dermal papilla compresses the nerve endings between the stacked capsular cells of a Meissner corpuscle, whereas pressure on a neighboring papilla is not nearly so effective. Meissner corpuscles are abundant in the skin of fingertips, and they and Merkel endings are largely responsible for our ability to perform fine tactile discriminations with our fingertips (Fig. 9-9; see also Fig. 9-18). Most animals have their own species-specific patterns of distribution of receptors, with specializations in functionally important parts of the body. Rats and cats have elaborate arrays of receptors surrounding their whiskers and large areas of somatosensory cortex devoted to their whiskers. Elephants mind their trunks. Other animals have other patterns (Box 9-1).

Figure 9-9 Correlation of spatial resolution and number of cutaneous receptors in different areas of the human hand. Spatial resolution (the reciprocal of the two-point discrimination threshold) was determined in psychophysical experiments by touching humans with two points and determining the minimum separation needed for them to be recognized as two separate points; this separation is less than 2 mm for fingertips but more than 8 mm for the palm of the hand. Correspondingly, there are many more Meissner corpuscles and Merkel endings per cm² in the fingertips than in the palm.

(Modified from Vallbo ÅB, Johansson RS: Hum Neurobiol 3:3, 1984.)