The Somatosensory System - a brief overview

Principles of Sensory Coding

The sensory system is a part of our nervous system that processes sensory information. Through the five sense-doors, it is responsible for giving direct representations of the outside world. Some key principles govern the way our sensory system works. First, the sensory system extracts sensory information arriving based on the type of stimulus (modality), location, intensity, and duration. Second, the arriving stimulus creates certain perceptual experiences within us. The conversion of stimulus information into neural signals by the sensory system is called sensory coding. Arriving external stimuli will be captured as energy by specialized peripheral "sensors" called receptors. These sensitive organs can be found in all five senses: eyes, ears, nose, tongue, and bodily receptors. The basic sensory modalities include light, sound, smell, taste, temperature, and pressure. Law of receptor specificity says that different nerve fibers are dedicated to different sensory modalities. 

• Location coding: we are aware of a specific site of touching or pressure (location of the stimulus) as it impinges a specific receptor on the skin. Such receptor is broadly called the receptor field. This receptor field in turn makes a specific connection in the brain such that different areas in the brain are stimulated. Location coding is not preserved in the chemosensory modality. 
• Intensity coding: the greater the stimulus intensity beyond a certain threshold of detection (see: Psychophysics), the greater the output of the receptor. More importantly, the intensity of a stimulus is coded in frequency terms -- the greater the stimulus intensity, the greater the discharge rate of action potential. However, other non-sensory factors are able to influence this frequency: fatigue, motivation, etc. 
• Duration coding: our awareness stay as long as the stimulus exists. To some senses, the awareness of a stimulus may decline over time, a process called adaptation, and it is caused by the way ion channels work. E.g. we perceive the cushion-like feeling when we first sit on the chair, but that awareness gradually disappears. 
• From the receptors, signals are transmitted through several anatomically distinct pathways following a concept of parallel pathways. Parallel processing is an important feature of hierarchical sensory processing. Brain compartments that process sensory information have an orderly, topographic, structured representation. The sensory systems do not enjoy equal representation in the brain (e.g. the somatotopic map of touch perception). 

The visual system, centered on the Occipital Cortex, is arguably the most dominant percept. Among the senses, however, the somatosenses or the perception of 'body' is intimately related to the motor cortex to plan and guide goal-directed movement. This post attempts to summarize their neural substrates and behavior.

There are three types of somatosenses based on the modality, the type of stimuli our brain perceives. First, the mechanoreceptors detect touch, pain, and temperature stimuli, and are embedded inside the dermal layer of the skin. A wide variety of receptors are able to detect vibration, stretch, pressure, shape, and texture. The proprioception & kinesthesia, embedded mainly in the joints and muscles, detect the position and movement of the trunk and limbs. And lastly, the senses of the internal organs in the body detect pain sensation or discomfort.

Proprioception is one of the core themes in my lab. Originally thought only to be sensed by certain sensory neurons in the muscle, proprioceptive information is also received by other mechanoreceptors in the skin and muscles. There is a set of specialized sensory neurons coming from the muscles. Embedded deep inside the extrafusal fibers is a set of muscle spindles that carry Type Ia and II sensory neurons. They encode muscle length or stretch. When the muscles contract, however, they lose sensitivity and fire less. It is the gamma motor neurons that increase or offset the loss of sensitivity by introducing tension to the muscle spindle. Type Ia neurons, in particular, are sensitive to the change in the stretch over time or velocity. Type Ib sensory neurons originate in the tendon organ that encodes muscle tension, but not stretch or length. Microelectrode recording is able to distinguish their discharge pattern in response to a certain behavior manipulation.

Fig-1:  Major ascending pathways; taken from [3].        

The Ascending Pathways
The spinal cord plays a critical role as it contains massive highways from and to the brain. Cross-sectionally, the spinal cord is divided into the core grey matter (H-shaped butterfly) surrounded by white matter. The ventral portion of the grey matter contains cell bodies of alpha motor neurons. The dorsal portion contains sensory axons and cell bodies of interneurons. The spinal cord is important for short-latency reflex.

The spinal cord serves as the base in the motor hierarchy but it is the first station of the sensory inflow to the brain. 

Sensory information from the trunk and limbs enters the spinal cord and travels up to the cerebral cortex through the thalamus, the ventral-posterior-lateral nucleus. 

The pathways called the ascending sensory pathways, work in parallel to ensure timely information delivery. The cell bodies of the sensory receptors are collectively called the dorsal root ganglion.

Two sensory pathways are present depending on the type of modality. The more precise receptors (touch, kinesthesia) ascend to the medulla and the thalamus through dorsal columns. The axons cross at the medulla forming the medial lemniscus to the opposite side of the brain, just like the descending motor pathways and hence contralateral in nature. The second pathway is dedicated to more poorly localized percepts such as pain and temperature. Upon entering the gray matter, the axons immediately cross and form the spinothalamic tract up to the thalamus. This tract is part of the bigger anterolateral pathways.

Thalamus as a Relay System
Thalamus is an important structure near the middle of the cerebral hemisphere, medial and caudal to the basal ganglia. It has two lobes in both left/right hemispheres and receives information from one part of the central nervous system (e.g. basal ganglia, cerebellum, motor cortex) and sends it to the other region through projection fibers. It is an essential link between sensory receptors and the cortex for all modalities except olfaction. This oval-shaped structure is situated bilaterally and consists of several distinct nuclei.

There are two types of thalamic nuclei in the thalamus: specific and non-specific. The name arises due to the way the nucleus is related to different brain regions. The non-specific nuclei, mainly in the internal medullary lamina, possess complicated input-output connections and does not bear selectivity or specificity to a certain cortical region or cortical function. The specific thalamic nuclei, whose outputs are excitatory (glutamatergic system), consist of four main divisions:

1. Anterior division: consists only of one nuclei and is linked to the mammillary bodies (part of the hypothalamus) and hippocampal formation, the cingulate and frontal lobe.
2. Medial division: it is connected to the basal ganglia, amygdala, and the midbrain, been implicated in memory.
3. Ventral division: the division that is very important for sensorimotor-related behavior. The ventro-anterior and ventro-lateral nuclei send information from the basal ganglia and cerebellum to motor cortex. We just mention the area that's involved in sending somatosensory information to S1. 
4. Posterior division: this area is mainly for the auditory (medial geniculate nucleus) and visual system (lateral geniculate nucleus); there is also the pulvinar nuclei that carry various functions and are interconnected to the parietal and occipital lobe.

The thin outer layer of the thalamus, called the reticular nucleus, is thought to provide inhibitory feedback. This means that the thalamus is not merely a congregation of relays but able to perform some information processing in the nuclei.

The Somatosensory Cortex
Axons in the ventral-posterior-lateral nucleus terminate primarily in the postcentral gyrus, or more popularly now as the primary somatosensory cortex or S1. It is situated between the central sulcus and postcentral sulcus, caudal to the primary motor cortex. We gain insights into this area by using the same electrical stimulation technique similar to the ones used in cortical motor experiments. Penfield found that these neurons are sensitive to tactile stimulation of the skin surface. Other scientists e.g. Woolsey, Kaas, etc. performed similar experiments on monkeys.

Like the primary motor cortex, the bodily representation in S1 is arranged in an orderly fashion or somatotopic. It turns out that the topography is not simple and the postcentral gyrus is further subdivided into Area 3a, 3b, 1, and 2 (correspondingly BA-3a/b, BA-1, and BA-2). Area 3 processes the basic somatosensory information and is arguably the only S1-proper as it receives the most projections from the thalamus. Neurons in BA-3a/b are found to have the smallest receptive fields. So what are the functional divisions of the somatosensory cortex?

• Proprioceptive sensory information from the muscles and joints is represented in Area 3a.
• Cutaneous and tactile information is represented in Area 3b.
• Area 3a/3b sends projections to Area 1 where higher-order processing takes place.
• Lastly, Area 2 is where information from Area 1 is fused with information from muscles and joints to facilitate richer tactile recognition related to grasping such as size and shape, and joint information while moving. The cells have the largest receptive fields.

Fig-2:  The primary somatosensory cortex; adapted from [2]. Note how the coronal section reveals BA-4 as well.

The cortical-body mapping is represented by the homunculus map. Just like M1, the larger the area in S1 of a certain body map, the greater the number of 'computational efficiency' power involved. For example: our highly discriminative sense of touch in the index finger is due to the large area in S1 dedicated to processing somatosensory stimuli from this part of the body. By virtue of synaptic plasticity, it is important to note that the mapping can be modified by experience. Experiments in monkeys (e.g. Jenkins and Merzenich, et al., 1990) focusing on tactile sensation have shown that the cortical representation of the digits expands after repeated training or usage of that digits.

What's next? S1 and beyond

From the primary area, somatosensory information is transmitted to secondary areas such as the second somatosensory area (SII), insula, and parietal association areas. Okie, honestly their functionalities are rather vague and mixed. The second somatosensory cortex (SII, or S2) is located on the upper ceiling of the lateral fissure, an area called the parietal operculum. It receives inputs from all four divisions of the primary somatosensory cortex. These inputs appear to be crucial for if they are removed, SII will not elicit any response to tactile stimulation. Removal of SII neurons, on the other hand, do not influence neural response in S1. SII has projections to the insular cortex and temporal areas associated with tactile memory. One function of the insular cortex in body awareness is in understanding and judging pain.

The somatosensory cortex is also tightly linked to other, more posterior areas in the parietal lobe. Areas such as BA-5 and BA-7 receive inputs from S1 and are important in guiding movements, i.e. reaching and grasping. However, to make movements, we need visual inputs and proper decision-making. The integration of visual and somatosensory codes occurs in the posterior parietal cortex and it is often called the somatosensory association areas. The areas send projections to the frontal lobe, parahippocampal region, cingulate gyrus, etc. for higher-order cognition and learning. These areas integrate sensory information of multiple modalities and hence they are multimodal.

Fig-3:  Relationship between S1 and the association sensory cortex of the brain; taken from [1]. It can be seen that neurons in S1 project to M1, and the so-called secondary motor and somatosensory cortices.

Final remark: the homunculus

Homunculus describes the somatotopic mapping of afferent and efferent projections that are responsible for our movement and bodily senses. Typically, a large area of the body in the brain corresponds to higher processing resources in the brain (and vice versa). Humans are well-known to possess good fine motor skills as shown by the large hand representation in the motor and somatosensory cortices. See below.

Fig-4: Homunculus of the somatosensory (afferent) and motor (efferent) projections.

As mentioned, the primary motor cortex (M1) receives a large projection from S1. Both areas are also organized in an orderly somatotopic fashion. One advantage of having the motor and somatotopic maps in close proximity (i.e., on either side of the central sulcus) is that it permits a more precise registration in the connectivity. The specificity in terms of bodily representation between M1 and S1 is reflected by the homotopic connection.

This connection is understandable given how closely the two systems must cooperate when we physically interact with an object. Indeed, the projections of S1 to M1 are organized in a homotopic fashion—that is, a given part of the motor cortex receives projections from the same part on the body map of the somatosensory cortex. Such interaction requires processes that rely on feedback signals from tactile receptors in the skin and proprioceptive receptors in the muscles.

References

[1]  Chapter 18 - The Functional Organization of Perception and Movement. In Kandel E.R. et. al. (2000). Principles of Neural Science 4e, McGraw-Hill.

[2]  Figure 20-1 (p.384) and Figure 23-1 (p.453). In Kandel E.R. et. al. (2000). Principles of Neural Science 4e, McGraw-Hill.
[3]  Chapter 7 - Audition, Chemical, Body Senses. In Carlson, Neil R. (2013). Physiology of Behavior 11e. Pearson Education.

Hierarchy of Sensorimotor System - a brief overview

The Overall Organization
Neural circuits involved in movement production are very complex. Motor commands are sent to the corresponding muscles through the motor system or efferent connection (efferent - exit the brain, output). In turns, the sensation from the peripheral system, e.g. the visual system, bodily touch, and proprioception, make up what we called the sensory system or sensory afferent (afferent - affect the brain, input). 

Sensory and motor systems are organized hierarchically. We have the spinal cord as the base, followed by the brainstem, and the cerebral cortex as the highest order. In addition, there are separate yet parallel processing pathways connecting these three so that information is processed in a timely fashion. A major function of the somatosensory system is to provide information for the purposeful movement of our limbs and body in relation to objects in the external world with which we interact. There are two critical sites where both systems make contact, each representing a different level of hierarchy: 

(1)  The spinal cord represents the lowest motor hierarchy that is stereotyped and repetitive.

(2)  The cerebral cortex at the level of the central sulcus provides voluntary control.

The spinal cord contains lower motor neurons
The spinal cord is composed of a central core region in the butterfly-shaped gray matter surrounded by white matter. The gray matter is subdivided into dorsal (posterior) and ventral (anterior) horns. The ventral horn contains cell bodies of alpha motor neurons, or lower motoneurons, that innervate muscles and produce movements. The intermediate zone is located in between the ventral and dorsal horn, and contains cell bodies of interneurons. In fact, it is the cell bodies that give the gray color to the structure. Low-level motor outputs are relatively stereotyped and the temporal accuracy is high. For instance, the spinal cord is where the simplest monosynaptic reflex circuit lies. Reflex movements are automatic and very fast, that is, with short latency (below 100 msec usually). Although technically reflexes do not involve the intervention of the cerebral cortex, central motor commands and cognitive processes have the capacity to alter synaptic transmission in spinal reflex pathways.

How does the circuit look like? The cell bodies of motor neurons that directly control and move muscles are located inside the ventral root of the spinal cord. Motor neurons of the ventral horn are modulated by interneurons, which in turn are controlled by two sources. The first source of input to the spinal motor networks is the somatosensory afferents whose cell bodies lie inside the dorsal root ganglion. Cell bodies of spinal interneurons are situated in the intermediate zone in between ventral and dorsal horns. Most reflexes, however, are polynsynaptic, meaning that there are more than one spinal interneuron involved. The second input source is the descending fibers within the spinal cord that carry motor commands issued by the cerebral cortex. Voluntary movements initiated by the motor cortex are therefore executed by the same network of spinal neurons that are involved in reflex behavior. For an anatomical perspective, see below.

Fig-1: Reflex mechanisms are produced by the sensorimotor system at the level of the spinal cord.

The brainstem consists of three divisions

The 3 divisions of the brainstem include the midbrain, medulla, and pons. Complex reflexes and rhythmic movements such as breathing, heart rate, and alertness occur in the brainstem. To some extent, balance and postural control recruit brainstem nuclei. Most autonomic systems involve the brainstem. Voluntary motor behavior also depends on various motor nuclei in the brainstem bilaterally, e.g. the red nuclei, vestibular nuclei, and the reticular formation. Each nucleus is uniquely connected to the spinal pathways both in ascending and descending manner. The details won't be discussed here.

The highest level of motor behavior is the cerebral cortex of the forebrain. This "controller" collects and integrates sensory information and is influenced by memory, subcortical modulation (the basal ganglia), and error correction (the cerebellum).

Why is the hierarchical structure important?
There is a considerable amount of time delay due to multiple connectivities in between. This problem, fortunately, is already solved by the hierarchical organization itself. For instance, when you want to flex your arm, there is this set of commands sent down from the motor cortex. This command will, at the same time, inhibit the opposing extensor muscles through the inhibitory interneuron that is activated during the stretch reflex. The variety of low-level circuits in the spinal cord and brainstem simplify the commands that the cortex has to send. Just like the director of the company instructs the managers and workers, in the same way, the motor cortex makes use of the simpler circuits by exciting some connections and inhibiting the rest. In this way, temporal details and precision will be left with the low-level motor neurons.

The Descending Pathways
The motor cortex sends commands to the spinal cord through axons projecting downwards, also known as the upper motor neurons. These neurons project directly and indirectly through various descending pathways situated alongside afferent sensory ascending pathways. The uncovering of such anatomical connections is not an easy feat, but thanks to studies by e.g. Lawrence and Kuypers (1968), we now know there are two main motor pathways mentioned below. The corticospinal tract is the only direct descending pathway from the motor cortex. Axons in this tract synapse directly with the alpha motor neurons of the skeletal muscle. Other pathways go through the brain stem and interact with the nuclei there, implying there is a certain degree of neuronal modulation involved. Refer to Fig-2.

1. The lateral group: the lateral corticospinal tract, corticobulbar tract, and rubrospinal tract. This group is primarily involved in making an independent goal-directed movement of distal limbs. This is important for reaching and object manipulation.
2. The ventromedial group: the anterior corticospinal tract, vestibulospinal tract, reticulospinal, and tectospinal tract. This group primarily controls the more proximal muscles and trunk related to postural control and locomotion.

Fig-2: The lateral (left) and medial (right) descending pathways of the voluntary movement; picture from [2]. 

The corticospinal tract consists of axons of motor neurons with cell bodies situated in the regions of the primary motor cortex that control the limbs and trunk. These neurons are called the Betz cells, which are unique to the motor cortex, and are the largest and longest neurons in the nervous system. They travel down from the cortex forming pyramidal tracts that terminate in the grey matter part of the spinal cord. The axons then cross over or decussate at the caudal medulla. Those which travel to the contralateral columns of the spinal cord form the lateral corticospinal tract and are associated with distal limbs, fingers, lower feet, and toes. Those which stay ipsilaterally are called the anterior corticospinal tract and are associated with the trunk and upper leg.

Note that if you read electrophysiology and monkeys literature, you may encounter different terms carrying the same meaning, that is, cortical motor neuron whose cell body resides in the cortex Layer V: pyramidal tract neuron (PTN) or upper motor neuron (as opposed to the alpha or lower motor neuron). A part of these neurons that carries direct connections with the lower motor neurons is called corticomotorneurone (CM cells).

The corticobulbar tract projects to the cranial nerves and controls facial muscles, neck, and tongue (refer back to the homunculus drawing!) The reticulospinal tract is associated with motor neurons whose cell bodies are located in the reticular formation, a network of nuclei occupying the core of the brainstem from the upper midbrain to the lower medulla. This structure is related to various tasks such as movements, arousal & sleep, and some complex reflexes. Neurons in this area control more automatic movement such as postural adjustment, breathing, sneezing, coughing.

The final common pathway:
Coined by Sherrington, this term refers to the lower motor neurons that innervate the skeletal muscle to induce movements. It is named 'common' in the sense that no matter what descending tract the axons originated, eventually, they will synapse in the ventral horn with the alpha motor neurons. One neuron can make contact (innervate) to 5 - 1000 muscle fibers. As a whole, the lower motor neuron and its target muscle are called the motor unit.

There are different sizes of cell bodies. Smaller neurons have smaller axons and thus higher total resistance. This, in turn, causes the post-synaptic potential to reach the threshold more easily. Innervation of the alpha motor neurons to muscles vary in quantity. The size principle of the motor unit recruitment states the following:

1. Muscle fibers targeted by the small alpha motor neurons are recruited (activated) first. With increasing force demand, muscle fibers targeted by large motor neurons will then start to be active.
2. Muscle fibers capable of producing large force get fatigued easily and they are fast-twitch. These fibers are able to generate different forces quickly. Conversely, muscles that produce smaller force are slow-twitch fibers, but more fatigue-resistant muscle fibers.
3. Small motor neurons innervate fewer muscle fibers. Larger neurons innervate more fibers. 

More on reflexes:

A large body of research dedicated to reflex patterns exists. Here, I just wanna summarize some famous reflexes, e.g. the withdrawal reflex, knee-jerk reflex. These are examples of the stretch reflex, also known as a myotactic reflex (roughly 30 – 80 msec latency). It happens when the muscle contracts in direct response to its stretch. 

Another form of reflexes called the long-loop reflexes are in response to somatosensory stimuli that are believed to operate via the cerebral cortex, hence the term transcortical reflexes. By definition, long loop reflexes occur at 60 – 120 msec latencies too long to be mediated by the circuits within the spinal cord yet too short to be mediated volitionally. Voluntary movements occur probably with > 150 msec latency. 

The Hoffman reflex, or H reflex, is a type of reflex elicited through electrical stimulation. Hence this reflex is generally considered the electrical equivalent of the knee-jerk, differing only in that the H reflex bypasses muscle spindle mechanisms. The H reflex can be used to assess the response of the nervous system to various neurologic conditions, neuromuscular injury, training, etc. 

References
[1]  Chapter 33 - The Organization of Movement. In Kandel E.R. et. al. (2000). Principles of Neural Science 4e, McGraw-Hill.
[2]  Chapter 8 - Control of Movement. In Carlson, Neil R. (2013). Physiology of Behavior 11e, Pearson Education.