Sensory Systems/Somatosensory System

Sensory Organs

Our somatosensory system consists of sensors in the skin and sensors in our muscles, tendons, and joints. The receptors in the skin, the so called cutaneous receptors, tell us about temperature (thermoreceptors), pressure and surface texture (mechano receptors), and pain (nociceptors). The receptors in muscles and joints provide information about muscle length, muscle tension, and joint angles. (The following description is based on lecture notes from Laszlo Zaborszky, from Rutgers University.)

Sensory Organ Components

Cutaneous receptors

Mechanoreceptors

Receptors in the human skin: Mechanoreceptors can be free receptors or encapsulated. Examples for free receptors are the hair receptors at the roots of hairs. Encapsulated receptors are the Pacinian corpuscles and the receptors in the glabrous (hairless) skin: Meissner corpuscles, Ruffini corpuscles and Merkel’s disks.

Sensory information from Meissner corpuscles and rapidly adapting afferents leads to adjustment of grip force when objects are lifted. These afferents respond with a brief burst of action potentials when objects move a small distance during the early stages of lifting. In response to rapidly adapting afferent activity, muscle force increases reflexively until the gripped object no longer moves. Such a rapid response to a tactile stimulus is a clear indication of the role played by somatosensory neurons in motor activity.

The slowly adapting Merkel's receptors are responsible for form and texture perception. As would be expected for receptors mediating form perception, Merkel‘s receptors are present at high density in the digits and around the mouth (50/mm2 of skin surface), at lower density in other glabrous surfaces, and at very low density in hairy skin. This innervations density shrinks progressively with the passage of time so that by the age of 50, the density in human digits is reduced to 10/mm2. Unlike rapidly adapting axons, slowly adapting fibers respond not only to the initial indentation of skin, but also to sustained indentation up to several seconds in duration.

Activation of the rapidly adapting Pacinian corpuscles gives a feeling of vibration, while the slowly adapting Ruffini corpuscles respond to the lataral movement or stretching of skin.

	Rapidly adapting	Slowly adapting
Surface receptor / small receptive field	Hair receptor, Meissner's corpuscle: Detect an insect or a very fine vibration. Used for recognizing texture.	Merkel's receptor: Used for spatial details, e.g. a round surface edge or "an X" in brail.
Deep receptor / large receptive field	Pacinian corpuscle: "A diffuse vibration" e.g. tapping with a pencil.	Ruffini's corpuscle: "A skin stretch". Used for joint position in fingers.

Nociceptors

Nociceptors have free nerve endings. Functionally, skin nociceptors are either high-threshold mechanoreceptors or polymodal receptors. Polymodal receptors respond not only to intense mechanical stimuli, but also to heat and to noxious chemicals. These receptors respond to minute punctures of the epithelium, with a response magnitude that depends on the degree of tissue deformation. They also respond to temperatures in the range of 40-60oC, and change their response rates as a linear function of warming (in contrast with the saturating responses displayed by non-noxious thermoreceptors at high temperatures).

Pain signals can be separated into individual components, corresponding to different types of nerve fibers used for transmitting these signals. The rapidly transmitted signal, which often has high spatial resolution, is called first pain or cutaneous pricking pain. It is well localized and easily tolerated. The much slower, highly affective component is called second pain or burning pain; it is poorly localized and poorly tolerated. The third or deep pain, arising from viscera, musculature and joints, is also poorly localized, can be chronic and is often associated with referred pain.

Thermoreceptors

The thermoreceptors have free nerve endings. Interestingly, we have only two types of thermoreceptors that signal innocuous warmth and cooling respectively in our skin (however, some nociceptors are also sensitive to temperature, but capable of unamibiously signaling only noxious temperatures). The warm receptors show a maximum sensitivity at ~ 45°C, signal temperatures between 30 and 45°C, and cannot unambiguously signal temperatures higher than 45°C , and are unmyelinated. The cold receptors have their maximum sensitivity at ~ 27°C, signal temperatures above 17°C, and some consist of lightly myelinated fibers, while others are unmyelinated. Our sense of temperature comes from the comparison of the signals from the warm and cold receptors. Thermoreceptors are poor indicators of absolute temperature but are very sensitive to changes in skin temperature.

Proprioceptors

The term proprioceptive or kinesthetic sense is used to refer to the perception of joint position, joint movements, and the direction and velocity of joint movement. There are numerous mechanoreceptors in the muscles, the muscle fascia, and in the dense connective tissue of joint capsules and ligaments. There are two specialized encapsulated, low-threshold mechanoreceptors: the muscle spindle and the Golgi tendon organ. Their adequate stimulus is stretching of the tissue in which they lie. Muscle spindles, joint and skin receptors all contribute to kinesthesia. Muscle spindles appear to provide their most important contribution to kinesthesia with regard to large joints, such as the hip and knee joints, whereas joint receptors and skin receptors may provide more significant contributions with regard to finger and toe joints.

Muscle Spindles

Mammalian muscle spindle showing typical position in a muscle (left), neuronal connections in spinal cord (middle) and expanded schematic (right). The spindle is a stretch receptor with its own motor supply consisting of several intrafusal muscle fibres. The sensory endings of a primary (group Ia) afferent and a secondary (group II) afferent coil around the non-contractile central portions of the intrafusal fibres. Gamma motoneurons activate the intrafusal muscle fibres, changing the resting firing rate and stretch-sensitivity of the afferents.

Scattered throughout virtually every striated muscle in the body are long, thin, stretch receptors called muscle spindles. They are quite simple in principle, consisting of a few small muscle fibers with a capsule surrounding the middle third of the fibers. These fibers are called intrafusal fibers, in contrast to the ordinary extrafusal fibers. The ends of the intrafusal fibers are attached to extrafusal fibers, so whenever the muscle is stretched, the intrafusal fibers are also stretched. The central region of each intrafusal fiber has few myofilaments and is non-contractile, but it does have one or more sensory endings applied to it. When the muscle is stretched, the central part of the intrafusal fiber is stretched and each sensory ending fires impulses.

Numerous specializations occur in this simple basic organization, so that in fact the muscle spindle is one of the most complex receptor organs in the body. Only three of these specializations are described here; their overall effect is to make the muscle spindle adjustable and give it a dual function, part of it being particularly sensitive to the length of the muscle in a static sense and part of it being particularly sensitive to the rate at which this length changes.

1. Intrafusal muscle fibers are of two types. All are multinucleated, and the central, non-contractile region contains the nuclei. In one type of intrafusal fiber, the nuclei are lined up single file; these are called nuclear chain fiber. In the other type, the nuclear region is broader, and the nuclei are arranged several abreast; these are called nuclear bag fibers. There are typically two or three nuclear bag fibers per spindle and about twice that many chain fibers.
2. There are also two types of sensory endings in the muscle spindle. The first type, called the primary ending, is formed by a single Ia (A-alpha) fiber, supplying every intrafusal fiber in a given spindle. Each branch wraps around the central region of the intrafusal fiber, frequently in a spiral fashion, so these are sometimes called annulospiral endings. The second type of ending is formed by a few smaller nerve fibers (II or A-Beta) on both sides of the primary endings. These are the secondary endings, which are sometimes referred to as flower-spray endings because of their appearance. Primary endings are selectively sensitive to the onset of muscle stretch but discharge at a slower rate while the stretch is maintained. Secondary endings are less sensitive to the onset of stretch, but their discharge rate does not decline very much while the stretch is maintained. In other words, both primary and secondary endings signal the static length of the muscle (static sensitivity) whereas only the primary ending signals the length changes (movement) and their velocity (dynamic sensitivity). The change of firing frequency of group Ia and group II fibers can then be related to static muscle length (static phase) and to stretch and shortening of the muscle (dynamic phases).
3. Muscle spindles also receive a motor innervation. The large motor neurons that supply extrafusal muscle fibers are called alpha motor neurons, while the smaller ones supplying the contractile portions of intrafusal fibers are called gamma neurons. Gamma motor neurons can regulate the sensitivity of the muscle spindle so that this sensitivity can be maintained at any given muscle length.

Golgi tendon organ

Mammalian tendon organ showing typical position in a muscle (left), neuronal connections in spinal cord (middle) and expanded schematic (right). The tendon organ is a stretch receptor that signals the force developed by the muscle. The sensory endings of the Ib afferent are entwined amongst the musculotendinous strands of 10 to 20 motor units.

The Golgi tendon organ is located at the musculotendinous junction. There is no efferent innervation of the tendon organ, therefore its sensitivity cannot be controlled from the CNS. The tendon organ, in contrast to the muscle spindle, is coupled in series with the extrafusal muscle fibers. Both passive stretch and active contraction of the muscle increase the tension of the tendon and thus activate the tendon organ receptor, but active contraction produces the greatest increase. The tendon organ, consequently, can inform the CNS about the “muscle tension”. In contrast, the activity of the muscle spindle depends on the “muscle length” and not on the tension. The muscle fibers attached to one tendon organ appear to belong to several motor units. Thus the CNS is informed not only of the overall tension produced by the muscle but also of how the workload is distributed among the different motor units.

Joint receptors

The joint receptors are low-threshold mechanoreceptors and have been divided into four groups. They signal different characteristics of joint function (position, movements, direction and speed of movements). The free receptors or type 4 joint receptors are nociceptors.

Proprioceptive Signal Processing

Feedback loops for proprioceptive signals for the perception and control of limb movements. Arrows indicate excitatory connections; filled circles inhibitory connections.

Modelling muscle spindles and afferent response

The response of the muscle spindles in mammals to muscle stretch has been thoroughly studied, and various models have been proposed. However, due to the difficulty in obtaining accurate data of the afferent and fusimotor responses during muscular movement, these models have usually been quite limited. For example, several of the earliest models account only for the afferent response, ignoring the fusimotor activity.

Mileusnic et al. (2006) model

One recent model, developed by Mileusnic et al. (2006), portrays the muscle spindle as consisting of several (typically 4 to 11) nuclear chain fibres, and two different nuclear bag fibres, connected in parallel as shown here in the figure below. The muscle fibres respond to three inputs: fascicle length, dynamic fusimotor input and static fusimotor input. The $bag_1$ fibre is mainly responsible for detecting dynamic fusimotor input, while the $bag_2$ and chain fibres are mainly responsible for detecting static fusimotor input. All fibres respond to changes in the fascicle length, and are modelled in largely the same way but with different coefficients to account for their different physiological properties. The responses of the three types of fibres are summed to generate the primary and secondary afferent activities. The primary afferent activity is affected by the response of all three types of muscle fibres, while the secondary afferent activity only depends on the $bag_2$ and chain fibre responses.

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Hasan (1983) model

Another comprehensive model of muscle spindles was proposed by Hasan in 1983 . This representation of muscle fibres and spindles is based closely on their physical properties. The muscle spindle is represented as two separate regions connected in series: sensory and non-sensory. The firing rate of the spindle afferent depends on the state of the two regions. The lengths of the two regions can be labelled $z(t)$ for the sensory and $y(t)$ for the non-sensory region. The tension $f(t)$ in the two regions is equal, since they are placed in series. The sensory zone can be assumed to act like a spring (equation (3)), while in the non-sensory region, tension is a non-linear function of $y(t)$ (equation (2) derived by Hasan).

$f(t) = k_1(y(t)-c)(1+[\frac{y'(t)}{a}]^{\frac{1}{3}}) \qquad \qquad \text{(2)}$
$f(t) = k_2z(t) \qquad \qquad \qquad \qquad \qquad \qquad \text{(3)}$

The total length of the muscle spindle, x(t) is the sum of the length of the two regions (equation (4)).

$x(t) = z(t) + y(t) \qquad \qquad \qquad \qquad \qquad \text{(4)}$

Using this substitution and rearranging, we can derive the following expression for the length of the sensory zone (equation (5)):

$z'(t) = x'(t) - a(\frac{bz(t) - x(t) + c}{x(t) - z(t) - c})^3 \qquad \text{(5)}$

Here, parameter $a$ represents the sensitivity of the tension to to velocity in the non-sensory zone, parameter $b = (k_1+k_2)/k_1$ and parameter $c$ determines the zero-length tension which influences the background firing rate of the afferent. The length of the sensory zone depends not only on the current length and velocity of the spindle, but on the history of the length changes.

The firing rate, $g(t)$ in Hasan's model depends on a combination of the sensory zone length and its first derivative (equation (6)), with an experimentally derived weighting.

$g(t) = z(t) + 0.1z'(t) \qquad \qquad \qquad \qquad \text{(6)}$

Model parameters

Approximate values for the model parameters a, b and c were suggested by Hasan (1983), and differ for voluntary and passive movements. A summary of these values is presented in the table below. Type of ending Condition A (mm/s) B C (mm)

Type of ending	Condition	A (mm/s)	B	C (mm)
Primary	Passive	0.3	250	-15
Primary	Gamma - dynamic	0.1	125	-15
Primary	Gamma - static	100	100	-25
Secondary	Passive	50	50	-20

In the model, these values are assumed to be static for the duration of a movement, however this is not believed to be the case.

Internal models of limb dynamics

In addition to modelling the response of muscle spindle afferents to muscle stretch, several groups have worked on modelling the signals which are sent from the brain to the spindle efferents in order for muscles to complete specific movements. The complexity here lies in the fact that the brain must be able to adapt to unexpected changes in the dynamics of planned movements, using feedback from the spindle afferents.

Studies in this area suggest that humans achieve this using internal models, which are built through an “error-feedback-learning” process, and transform planned muscle states into the motor commands required to achieve them. To generate the motor commands for a particular reaching movement, the brain performs calculations based on the expected dynamics of the planned movement. However, any unexpected changes in these dynamics while the movement is being executed (e.g. external strain placed on the muscle) will lead to errors in expected muscle length (Gottlieb 1994, Shadmehr and Muss-Ivaldi 1994). These errors are communicated to the brain through the muscle spindle afferents, which experience a different sensory state to what is expected. The brain then reacts to these error signals with short and long latency responses, which work to minimise the error, but cannot eliminate it completely due to the delay in the system.

Studies suggest that the error can be eliminated in a subsequent attempt at the movement under the same dynamics, and this is where the “error-feedback-learning” idea comes from (Thoroughman and Shadmehr 1999). The corrections which are generated by the brain form an internal model, which maps a desired action (in kinematic coordinates) to the necessary motor commands (as torques). This internal model can be represented as a weighted combination of basis elements:

$torque = \sum w_i g_i(\theta,\theta',\theta''...)$

Here each basis $g_i$ represents some characteristic of the muscle's sensory state, and the motor command is a “population code”. Population coding is a method of representing stimuli as the combined activity of many neurons (in contrast to rate coding). In order to use such a model, we need to know how the bases represent particular limb or muscle positions, and the neuronal firing rates associated with them. The bases can, in principle, represent every aspect of the state: position, velocity, acceleration and even higher derivatives. However, this high dimensionality makes it very difficult to derive relationships experimentally between each dimension of the bases and the firing rates.