The Somatosensory System I: Tactile Discrimination and Position Sense

Peripheral Mechanoreceptors

The first step in evoking somatic sensations of touch is the activation of peripheral mechanoreceptors. Mechanical pressure, such as skin deformation, is transduced into an electrical signal in the peripheral process of a primary afferent neuron (see Chapter 3 ). This leads to a depolarizing graded membrane potential across the membrane of the neuron. If this potential depolarizes the trigger zone, located at the first myelin segment of the axon, to threshold, an action potential is produced (see Chapter 3 ). In most receptors, transduction occurs between the mechanoreceptor and the subjacent primary afferent membrane. However, in some cases (i.e., Merkel cells), the nonneural cells of the receptor complex may influence their associated primary afferent axon by vesicular release of neurotransmitters or neuromodulators (e.g., glutamate, serotonin (5-hydroxytryptamine [5-HT], substance P, vasoactive polypeptide [VIP]). Upon release from the Merkel cell, these substances bind to specialized membrane receptor complexes and can alter sensory transmission.

Each morphologic type of mechanoreceptor responds to different tactile stimuli. Cutaneous tactile receptors ( Table 17.1 ; Fig. 17.1 ) are located in the basal epidermis and dermis of glabrous (palms, soles, lips) and hairy skin. These low-threshold mechanoreceptors may be encapsulated, such as Meissner, Pacinian, and Ruffini corpuscles, or unencapsulated, such as Merkel cell–neurite complexes (commonly referred to as Merkel cells ) and hair follicle receptors. Meissner corpuscles, some hair follicle receptors, and Pacinian corpuscles respond to transient, phasic, or vibratory stimuli. These receptors respond to each initial application or removal of a stimulus but fail to respond during maintained stimulation. Consequently, they are rapidly adapting (RA) receptors ( Fig. 17.2 A ). Hair follicle receptors are also capable of signaling motion, its direction or orientation, and its velocity.

Merkel cells, Ruffini corpuscles, and some hair follicle receptors signal tonic events such as discrete small indentations in the skin. They provide input related to both the displacement and velocity of a stimulus. They are also capable of encoding stimulus intensity or duration because they are slowly adapting (SA) and are active so long as the stimulus is present ( Fig. 17.2 A ). For example, Merkel cells are crucial to reading of Braille.

Deep tactile mechanoreceptors are found within the dermis of the skin, in the fascia surrounding muscles and bone, and in the periodontium. These receptors include Pacinian corpuscles, Ruffini corpuscles, and other encapsulated nerve endings located in the periosteum, the deep fascia, and the mesenteries. The receptors of this group respond to pressure, vibration ( Fig. 17.2 B; Table 17.1 ), skin stretch and distention, or tooth displacement.

Proprioceptive receptors ( Table 17.2 ; Fig. 17.1 ) are located in muscles, tendons, and joint capsules. These receptors include muscle spindles and their associated nuclear bag-and-chain muscle fibers that are innervated by Ia and II afferent nerve fibers. The Golgi tendon organs and their group Ib fibers and the encapsulated Ruffini-type joint receptors also function in this capacity. They respond to static limb and joint position or to the dynamic movement of the limb ( kinesthesia ) and are important sources of information for balance, posture, and limb movement.

The accuracy with which a tactile stimulus is localized depends on the density of receptors and the size of their receptive fields ( Fig. 17.3 ). The greatest density of cutaneous tactile receptors is found on the tips of the glabrous digits and in the perioral region. Other regions, like the back, have much lower density, thus creating a receptor density gradient between various body parts. The receptive field is the area of skin innervated by branches of a somatic afferent fiber, the stimulation of which activates its receptors ( Fig. 17.3 ). Small receptive fields are found in areas such as the fingertips, where receptor density is high and each receptor serves an extremely small area of skin. In such regions, the individual is capable of discriminating small variations in a variety of sensory inputs. In other regions, receptor density is low and each receptor serves an expansive area of skin, creating large receptive fields with resultant reduction in discriminative ability.

At all levels of the tactile pathway, densely innervated body parts are represented by greater numbers of neurons and take up a disproportionately large part of the somatosensory system’s body representation. In this respect, there is an inverse relationship between the size of the receptive field and the representation of that body part in the somatosensory cortex. For example, the trunk, with its large receptive fields, has a small representation in the somatosensory cortex, whereas the fingers, with their small receptive fields, have a large representation in the somatosensory cortex (compare Fig. 17.3 with Figs. 17.10 and 17.11 ). As a result, the fingertips and lips provide the central nervous system with the most specific and detailed information about a tactile stimulus.

Primary Afferent Fibers

As initially described in Chapter 9 , somatic afferent fibers consist of (1) a peripheral process extending from the posterior root ganglion either to contact peripheral mechanoreceptors or to end as free nerve endings, (2) a central process extending from the posterior root ganglion into the central nervous system, and (3) a pseudounipolar cell body in the posterior root ganglion. The peripheral distribution of the afferent nerves arising from each spinal level delineates the segmental pattern of dermatomes. In clinical testing, these ribbon-like strips of skin are associated primarily with fibers and pathways that convey pain and thermal information; they are considered in Chapter 18 .

Peripheral nerves are classified by two schemes. One is based on their contribution to a compound action potential (A, B, and C waves) recorded from an entire mixed peripheral nerve (e.g., sciatic nerve) after electrical stimulation of that nerve. The other scheme specific to cutaneous fibers (e.g., lateral antebrachial cutaneous nerve, sural nerve) is based on fiber diameter, myelin thickness, and conduction velocity (classes I, II, III, and IV) ( Table 17.3 ; Fig. 17.4 ). The two schemes are related because conduction velocity determines a fiber’s contribution to the compound action potential. Discriminative touch, vibratory sense, and position sense are transmitted by group Ia, Ib, and II fibers ( Tables 17.1 and 17.2 ). The compound action potential and conduction velocity of nerve fibers is often used as a diagnostic test in the evaluation of peripheral nerve disease, for instance, multiple sclerosis and peripheral neuropathies.

Spinal Cord and Brainstem

On the basis of cell size and fiber diameter, primary sensory fibers are categorized as large and small. Large-diameter fibers subserve discriminative touch, flutter-vibration, and proprioception (groups Ia, Ib, II, and Aβ; Tables 17.1 and 17.2 ). They enter the spinal cord via the medial division of the posterior root (see Chapter 9 ) and then branch ( Fig. 17.5 ). One set of branches terminates on second-order neurons in the spinal cord gray matter at, above, and below the level of entry. These branches contribute to a variety of spinal reflexes and to ascending projections such as postsynaptic posterior column fibers. The largest set of branches ascends cranially and contributes to the formation of the gracile and cuneate fasciculi. These fiber bundles are collectively termed the posterior columns owing to their position in the spinal cord ( Figs. 17.5 to 17.7 ).

Within the posterior columns, fibers from different dermatomes are organized topographically. Sacral level fibers assume a medial position, and fibers from progressively more rostral levels (up to thoracic level T6) are added laterally to form the gracile fasciculus ( Figs. 17.5 and 17.6 ). Thoracic fibers above T6 and cervical fibers form the laterally placed cuneate fasciculus in the same manner. Thus the lower extremity is represented medially and the upper extremity is represented laterally within the posterior columns ( Figs. 17.5 and 17.6 ). Compromise of blood flow in the posterior spinal artery, which supplies the posterior funiculus, or mechanical injury to the posterior columns (as in Brown-Séquard syndrome ) results in an ipsilateral reduction or loss of discriminative, positional, and vibratory tactile sensations at and below the segmental level of the injury. Symptoms indicative of damage to fibers of the posterior columns are also seen in tabes dorsalis ( progressive locomotor ataxia ). This disease is caused by infection with Treponema pallidum and is associated with neurosyphilis. The fibers of the posterior columns degenerate, and the patient has ataxia (related to the lack of sensory input, clinically referred to as sensory ataxia ), loss of muscle stretch (tendon) reflexes, and proprioceptive losses from the extremities. In sensory ataxia, the patient may also have a wide-based stance and may place the feet to the floor with force in an effort to create the missing proprioceptive input.

The posterior column nuclei, the gracile and cuneate nuclei, are found in the posterior medulla at the rostral end of their respective fasciculi. They are supplied by the posterior spinal artery ( Fig. 17.7 ). The cell bodies of the gracile and cuneate nuclei are the second-order neurons in the PCMLS. They receive input from first-order neurons having cell bodies in the ipsilateral posterior root ganglia ( Figs. 17.7 and 17.8 ). The gracile nucleus receives input from sacral, lumbar, and lower thoracic levels via the gracile fasciculus; the cuneate nucleus receives input from upper thoracic and cervical levels through the cuneate fasciculus.

In addition to the somatotopic organization of projections to the posterior column nuclei, there is a submodality segregation of tactile inputs within these nuclei. The second-order relay neurons are arranged into a core “clusters” region surrounded by a covering “shell” region that allows submodality segregation of the excitatory primary afferent input. Rapidly adapting and slowly adapting inputs terminate centrally within the core. Muscle spindle and joint inputs project preferentially to the rostral shell region. Pacinian corpuscle input is restricted to the caudal shell region.

The posterior column nuclei have an inner core region containing large projection neurons surrounded by a diffuse shell of small fusiform and radiating cells. The shell area contains interneurons responsible for feedback inhibition in the posterior column nuclei. This feedback alters activity of projection neurons of the inner core. The posterior column nuclei also receive descending axons from the contralateral primary somatosensory cortex and from the medullary reticular formation (nucleus reticularis gigantocellularis). The presence of non–posterior column inputs to these projection cells suggests that information received by the posterior column nuclei is not simply relayed but undergoes signal processing.

The second-order cells in the core region of the posterior column nuclei send their axons to the contralateral thalamus ( Figs. 17.7 and 17.8 ). In the medulla, the internal arcuate fibers, axons of cells in the posterior column nuclei, loop anteromedially and cross the midline as the sensory decussation, and ascend as the medial lemniscus on the opposite side. Fibers in the medial lemniscus that arise in the cuneate nucleus are located in superior portions of the medial lemniscus (and convey information from the upper extremity), and those from the gracile nucleus are located in its inferior parts (and relay data from the lower extremity) ( Figs. 17.6 and 17.8 ). The anterior spinal artery supplies the medial lemniscus in the medulla, and penetrating branches of the basilar artery ( paramedian and short circumferential ) supply it in the pons. Vascular damage at these brainstem levels leads to deficits in discriminative touch, vibratory, and positional sensibilities over the contralateral side of the body. As the medial lemniscus moves rostrally through the brainstem, it rotates laterally so that the upper extremity representation comes to lie medially and the lower extremity laterally in the pons ( Figs. 17.7 and 17.8 ). As the medial lemniscus traverses the midbrain, it is shifted laterally and posteriorly by the appearance of medial structures such as the red nucleus ( Figs. 17.7 and 17.8 ). The midbrain lesion in Fig. 17.9 compromised only the medial lemniscus on the right side and resulted in a loss of discriminative touch and proprioception on the patient’s left side. This patient did not experience the loss of any other modality. This somatotopic organization is generally maintained as the medial lemniscus terminates on cells in the ventral posterolateral nucleus (VPL) of the thalamus.

The postsynaptic posterior column pathway, a small supplemental pathway in humans that relays nondiscriminative tactile, as well as visceral nociceptive signals to supraspinal levels, consists of non–primary afferent axons carrying tactile signals in the posterior columns (see Fig. 17.14 ). The cells of origin of this pathway are located in laminae III and IV of the posterior horn. Axons of the second-order postsynaptic posterior column pathway travel in the posterior columns and together with other tactile primary afferent fibers terminate in the posterior column nuclei. Cells of these nuclei relay this postsynaptic posterior column input to the contralateral thalamus via the medial lemniscus. Although this pathway is small, it may provide the morphologic basis for the return of some tactile sensation after vascular lesions involving the PCMLS. This pathway has also been implicated as having an important role in relaying visceral nociceptive information. Recent evidence from clinical (positron emission tomography [PET] and functional magnetic resonance imaging [fMRI]) studies have shown that the visceral nociceptive axons in the postsynaptic posterior column pathway travel to the posterior column nuclei and to the cerebellum.

Ventral Posterior Nucleus

The ventral posterior nucleus, sometimes called the ventrobasal complex, is a wedge-shaped cell group located caudally in the thalamus. Its lateral border abuts the internal capsule, and ventrally it borders on the external medullary lamina. The ventral posterior nucleus is composed of the laterally located VPL and the medially located ventral posteromedial nucleus (VPM). Although these nuclei have also been termed the ventralis caudalis externus and ventralis caudalis internus in humans, the more widely used and recognized terms VPL and VPM are used in this book. The VPL is separated from the VPM by fibers of the arcuate lamina. The ventral posterior nucleus (VPM and VPL) is supplied by thalamogeniculate branches of the posterior cerebral artery, and compromise of these vessels can result in loss of all tactile sensation over the contralateral body and head ( Fig. 17.10 ).

The VPL receives ascending input from the medial lemniscus, and input to the VPM is from the trigeminothalamic tracts. Within the VPL, medial lemniscal fibers from the contralateral cuneate nucleus terminate medial to those from the gracile nucleus. As a result, the representation of the lower extremity is lateral, and that of the upper extremity is medial in the VPL ( Fig. 17.10 ). The representation of an individual body part is organized as a C-shaped lamina. Tactile signals are also represented in other thalamic nuclei receiving lemniscal input, including the ventral posterior inferior nucleus and the pulvinar and lateral posterior group.

In addition to their somatotopic organization, the medial lemniscal fibers that terminate in the ventral posterior nucleus are segregated on the basis of their functional properties. Rapidly and slowly adapting inputs terminate on different cell groups within the core region of the VPL. Pacinian inputs and inputs arising from joints and muscles are confined to a shell region on the posterior, rostral, and anterior edges of the nucleus. Individual lemniscal axons arborize in the sagittal plane to terminate on longitudinal cell clusters, called rods, in the VPL. This arrangement of inputs and target cells creates representations consisting of neurons with similar receptive fields and submodalities arranged along a rostrocaudal axis.

The VPL for the trunk and extremities (and VPM for the head) contains two populations of identified neurons. The first consists of large-diameter multipolar cells that give rise to axons that traverse the posterior limb of the internal capsule and terminate mainly in the primary (SI) and secondary (SII) somatosensory cortices. These thalamocortical cells and fibers are the third-order neurons in the PCMLS that provide excitatory (glutaminergic) input to the cortex. The second population consists of inhibitory (γ-aminobutyric acid [GABA]ergic) local circuit interneurons, which receive excitatory corticothalamic inputs and influence the firing rates of thalamocortical cells. In addition, these thalamocortical cells are also influenced by GABAergic input from the thalamic reticular nucleus and by excitatory (glutaminergic) corticothalamic fibers that arise in layer VI of the primary and secondary somatosensory cortices.

Primary Somatosensory (SI) Cortex

Axons from third-order thalamic neurons terminate in the primary somatosensory (SI) cortex ( Figs. 17.7, 17.10, and 17.11 ). This cortical region is bordered anteriorly by the central sulcus and posteriorly by the postcentral sulcus and comprises the postcentral gyrus and the posterior paracentral gyrus ( Fig. 17.12 ). The cortex contains a somatotopic representation of the body surface (a homunculus, or “little man”), which is laid out in a “foot to tongue” pattern along the medial to lateral axis ( Fig. 17.11 ). Body regions with a high density of sensory receptors, such as the hand and the lips, have a disproportionately large amount of cortical tissue dedicated to their central representation. In contrast, regions with low receptor density, such as the back, have small cortical representations ( Figs. 17.3 and 17.11 ). Blood supply to the SI cortical areas is provided by the anterior and middle cerebral arteries. Vascular lesions involving the middle cerebral artery produce tactile loss over the contralateral upper body and face, and those involving the anterior cerebral artery affect the contralateral lower limb.

On histologic examination, the primary somatosensory cortex is subdivided into four distinct areas; from anterior to posterior, these are Brodmann areas 3a, 3b, 1, and 2 ( Fig. 17.12 ). Area 3a is located in the depths of the central sulcus and abuts area 4 (primary motor cortex). Areas 3b and 1 extend up the bank of the sulcus onto the shoulder of the postcentral gyrus, whereas area 2 lies on the gyral surface and abuts area 5 (somatosensory association cortex).

Each of these four cytoarchitectural areas of the SI cortex receives submodality-specific inputs. Areas 3a and 2 are primarily targeted by neurons in the shell region of the VPL. They receive proprioceptive inputs arising from muscle spindle afferents (mainly area 3a), Golgi tendon organs, and joint afferents (mainly area 2). These two areas are capable of processing kinesthetic information related to muscle length and tension as well as static and transient joint position. Areas 3b and 1 are mainly targeted by neurons in the core region of the VPL. They receive cutaneous afferents from receptors such as Meissner corpuscles (RA) and Merkel cells (SA). In addition to receiving input that originates from cutaneous touch receptors, such as Meissner and Merkel endings, areas 3b and 1 also receive input from cutaneous receptors that transmit information concerned with pain and thermal sensations. The anterolateral system, the pain pathway, is described in Chapter 18 .

Small lesions in various parts of the somatosensory cortex may result in characteristic types of sensory losses. Lesions involving area 1 produce a deficit in texture discrimination, whereas damage to area 2 results in loss of size and shape discrimination ( astereognosis ). Injury to area 3b has a more profound effect than does damage to either area 1 or 2 alone, producing deficits in both texture and size and shape discrimination. This difference suggests that there is hierarchical processing of tactile information in the SI cortex, with area 3b performing the initial processing and distributing the information to areas 1 and 2. However, lesions involving the somatosensory cortex usually include larger areas and frequently result in more global deficits, such as a loss of proprioception, position sense, vibratory sense, and pain and thermal sensations on the contralateral side of the body.