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Proprioception: The Forgotten

Sixth Sense
Chapter: Foot sensation, balance and Proprioception

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Published Date: July, 2015

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 eBooks

Foot Sensation, Balance and Proprioception

Nihan Kafa*
Gazi University, Faculty of Health Sciences, Department of Physiotherapy and
Rehabilitation, 06100 Ankara, Turkey
*Corresponding author: Nihan Kafa, PT, PhD, Gazi University, Faculty of Health
Sciences, Department of Physiotherapy and Rehabilitation, 06100 Ankara, Turkey,
Tel: +90 5069159113, E-mail: nkaratas@gazi.edu.tr

Abstract
The cutaneous mechanoreceptors are widely expanded throughout the plantar foot
[1]. Primary role of the plantar foot mechanoreceptors is thought that reacting a stimuli
arised from the external environment. However, sometimes these mechanoreceptors provide
proprioceptive information to keep the postural control to the central nervous system [2].
The maintanence of human postural control not only involves sensory information from
the visual, vestibular and proprioceptive receptors but also includes somatosensory
information from these cutaneous mechanoreceptors located on the soles of the feet. The
mechanoreceptors provide detailed information about contact pressures on the foot and
feeling the changes to body conformance [3]. Additionally, cutaneous afferents from the
plantar foot assure a neuronal population vector that codes the direction of the ankle
movement and contribute to cognizance of body in space and to upright human posture [4].
Therefore, it could be said that plantar foot cutaneous afferents contribute properly to the
reflex regulation of balance with additional proprioceptive input [5].

Keywords: Balance; Plantar Foot Sensation; Proprioception

Plantar Foot Sensation
The tactile system is combined with sensations of touch and pressure and more complex
sensations like vibration [6]. The sensory receptors responsible for tactile sensations present
in skin, a multilayered coating covering the whole body.
It is classifed into three specific types:
a. Globrous skin characterized by the skin of the palm and the soles of feet;
b. Hairy skin;
c. Mucocutaneous skin.
The different organisation of these three types of skin gives differences to their sensory
capabilities [7, 8].
Glabrous and hairy skin are formed by an outside layer called epidermis and inside
layer called the dermis. The dermis allocates the epidermis from the underlying muscle,
ligaments and bone [7]. Localization of all sensations to their point of origin is greatest at
the body surface, and increasingly decreased in deeper structures [2].

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 The peripheral basis of tactile sensations ensues by the activation of sensory receptors,
located in the skin, that are sensitive to mechanical stimuli. These mechanosensory
neurons, called mechanoreceptors, are complex in structure and responsible for mechano-
electric transmission to the central nervous system [7-9]. When a mechanical stimuli
applied to the skin surface, it causes stresses and strains within the skin. There are three
kinds of mechanical disturbance that cause a stimuli to the skin. The first is called the
incompressible shear wave. These waves travel obliquely with respect to the stimulus
existed to the surface of the skin. The second is the linear compression wave. These travel
normally with respect to the stimulus performed to the skin surface. In this type of stimuli,
stresses and strains are conveyed to the mechanoreceptors located in the dermis. The third
type of wave is a travelling wave that disseminates along the body surface from the point of
stimulus excitation. This wave of stimulation activates mechanoreceptors located away from
the point of skin stimulation [7].
The mechanoreceptors in the dermis that are innervated by the peripheral nerve fibres
originating in the spinal cord come in a variety of shapes and forms. All these cutaneous
sensory neurons can be classified based on their cell body sizes, axon diameter, degree of
myelination and axonal conduction velocities [10]. The four main types of mechanoreceptors
are Pacinian corpuscles, activated by heavy pressure and vibration; Meissners corpuscles,
activated by light touch and vibration; Merkels discs, activated by light touch and pressure
and Ruffini endings, activated by skin stretch [6, 7, 10-12]. The physiologic classification
of mechanoreceptors follows a two-class designation based on the receptors responses to
ramp-and-hold-like stimuli which is a stimuli that quickly indent and sustain in contact
with the mechanoreceptor. The two general names of these classes are Fast Adapting (FA,
also called quickly adapting and rapidly adapting) and Slowly Adapting (SA). There are
subclasses of FA and SA mechanoreceptors: FA I, FA II, SA I and SA II [7,10]. Generally
type I receptors are placed superficially in the skin and have small receptive fields. Type II
receptors are deeply placed and have wide and diffuse receptive fields [13]. The differences
in response properties for these four mechanoreceptor types can be seen in the Table 1. For
example FA I: respond commonly to the ramp portion of the stimulus; FA II only counters
to the corners of the ramp-and-hold stimulus. SA I: respond not only the ramp part of the
stimulus but also to the hold part with an irregular firing patern. Finally SA II demonstrates
a more regular firing rate and also have spontaneous activity [7].
Physiological Associated fiber
Skin type End organ/ ending type Optimal Stimulus Response properties
subtype (conduction velocity)
Glabrous Merkel cell
Indentation
SA I A (16-96 m/s)
Hairy Merkel cell

Glabrous Ruffini
SA II A (20-100 m/s) Stretch
Hairy Unclear

Glabrous Meissner corpuscle

FA I A (26-91 m/s) Longitudinal Lanceolate Skin movement
Hairy
ending

FA II A (30-90 m/s) Glabrous Pacinian corpuscle Vibration

Table 1: A comparison of physiologic characteristics of mechanoreceptors [10].

This classification scheme is independent from receptor anatomy. However, it has been
fairly well identified that the FA Is are the Meissner corpuscles that responds to best to light
touch, the FAIIs are the Pacinian corpuscles that responds to best to vibration, the SAIs are
the Merkel cell that responds to best to pressure and the SAIIs are the Ruffini endings that
responds to best to pressure [7,10,13].

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 When the whole body parts are examined, there are distinct differences in the relative
dispensation of receptors between skin regions . For example there are receptors without
fast adapting type II units in the face and there is a lack of a potential third type of slow
adapting receptor in the thigh. To examine the potential role of cutaneous mechanoreceptors
in standing balance, it is important to understand the properties of skin receptors in the
plantar surface of the foot [1].
The distribution and behaviour of glabrous cutaneous receptors in the human plantar
foot are different from hand [14]. A total of 104 cutaneous mechanoreceptors were found in
glabrous skin of the plantar foot [1]. These cutaneous receptors includes 15 slow adapting
type I (14 %), 16 slow adapting type II (15 %), 59 fast adapting type I (57 %), and 14 fast
adapting type II units (14 %). While all four receptor types are existing in the plantar foot ,
it is difficult to classify the SA receptors into types II and I. The receptive fields of the SAII
receptors are similar to that of the SAI receptors [1] (Figure 1).

Figure 1: Distribution of cutaneous mechanoreceptors in the foot sole [1].

Many different ways are used to measure the mechanoreceptor activation. Generally
vibration pressure threshold were used as a measure of somatosensation [6,15-18]. Other
measurements used are touch pressure sensation threshold, two-point discrimination,
pressure algometry, joint motion perception threshold, and active and passive joint position
sense [6,16-20]. Also, more extensive somatosensation measurements the Valk score and
the Neurological Disability Score (NDS) are used techniques, depending upon receptor type
[6]. The location of the receptors and the outline of the receptive fields could be determined
by using nylon monofilaments [1,21,22]. In the plantar foot, the location of the receptors
are widely distributed without an accumulation in the toes [1] (Figure 1). There are larger
receptive fields predominantly isolated on the plantar surface of the metatarsal-tarsal region
of the plantar foot [1]. The widespread distiribution of receptors throughout the plantar
foot indicate that skin receptors would be able to code for contact pressures, and hence the
position of the foot with the ground. Regions of the foot that lift the majority of the bodys
weight in loaded conditions, have the accumulation of receptors [1]. Interestingly, in the non-
contact area, longitudinal arch, there were a limited number of receptors documented [5].
Kennedy et al., [1] conducted a study to document the activity of cutaneous mechanoreceptors
in the glabrous skin of the plantar foot. It was found that skin receptors in the glabrous skin
of the plantar foot have elevated activation thresholds in comparison with the glabrous skin of
the hand. For example, the median activation thresholds for the FA I and FA II units in the foot
were 11.8 and 4.0 mN [1], respectively whereas 0.58 and 0.54 mN were reported for the hand
[23]. Additionally it was also found that there is an absence of background activity in any of the
cutaneous mechanoreceptors with the plantar foot in an unloaded position [1]. The fact that
there was no background activity in a natural, unloaded position suggests that any activity
from plantar foot receptors may be important for signalling that the foot is in contact with the
supporting surface [24]. Also the wide dispensation of receptors throughout the plantar foot

3
would ensure that skin receptors would be able to code for contact pressures, and hence the
position of the foot with the ground [1].
Beyond the mechanoreceptors, the sensory impulses are propagated centrally by
a population of afferent nerve fibers. The composition of the sensory nerve compound
action potential includes A myelinated fibers (3072 m/sec) that convey light touch,
proprioception, vibratory, and discriminative sensations, A lightly myelinated fibers (430
m/sec), and C-unmyelinated fibers (0.42 m/sec) [10, 25]. These peripheral nerve fibers
of the first neurons which have their associated soma in the Dorsal Root Ganglia (DRG)
[13,26]. The DRG neurons are T shaped structures, separate axonal projections that convey
the impulse centrally to the spinal cord through the dorsal roots [13]. As the fibers enter
the spinal cord, the large myelinated fibers undertake a more medial position. The more
lateral aspect of the bundle includes thinly myelinated and unmyelinated fibers. The spinal
cord gray matter consist of laminaes, that often represent separate nuclei with distinctive
functions. Lamina IV plays a role in light touch, for example [13,27]. The impulses
ascending in the fibers of the dorsal columns intercede sensations of touch, deep pressure,
vibration, proprioception, and sensory discrimination [13,27]. The dorsal columns generally
represent direct ways from the DRG neurons to the nuclei gracilis and cuneatus within the
brain stem. However, some of the primary afferents coursing in the dorsal columns send
projections to the propriospinal neurons in the dorsal horn, and some axons of second-
order neurons from the dorsal horn flow in the dorsal columns and end on dorsal column
nuclei [13]. Second order neurons in these nuclei feed information forward to the thalamus
and finally third order thalamocortical neurons project to the somatosensory cortex [10].
The mechanoreceptors related with light touch and pressure include the Fast Adapted (FA)
and Slow Adapted (SA) type I receptors. Tactile sensory nerve fibers have their first-order
neurons in the dorsal root ganglion and enter the spinal cord through the medial division of
the dorsal root. These fibers are generally thought to traverse the medial region of the dorsal
roots and enter the dorsal columns ascending to the contralateral thalamus. Third-order
neurons then ascend to somatosensory cortex for perception of the stimulus [13].

Balance
Balance, the continuum of controlling the center of gravity over the base of support
within a given sensory environment, is composed of several subcomponents and influenced
by several systems [28-30]. It is necessary for individuals to move about their environment
and successfully perform daily activities [29,31]. Human postural control is a complex
neuromusculoskeletal process including the sensory detection of body motions, integration
of sensorimotor information within the Central Nervous System (CNS), and programming
and execution of the appropriate neuromuscular responses [29,30] (Figure 2).

Neuromusular
Weighting of sensory input
Sensory responses:
detection of
body position Perception of
in space Central Nerv ous System: postural
alignment,
Integration of sensorimotor Postural
Visual
information Determination adjustments,
Vestbular
of motor response Eye movements,
Proprioception
Upper extremity
Audition
activities

Environment/past experience

Figure 2: The organization of the human balance system [30].

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 Balance is considered a complex motor skill reproduced from the interaction of multiple
sensorimotor processes [32]. The two main functions of postural control are postural
orientation and postural equilibrium [32]. Postural orientation includes the active control
of body alignment and tone to build up posture against gravity, support surface, visual
environment and internal references. Spatial orientation in postural control is based on the
explication of convergent sensory information from somatosensory, vestibular and visual
systems [33]. Additionally, the other function postural equilibrium involves the coordination
of sensorimotor strategies to stabilise the bodys Centre of Mass (CoM) during both self-
initiated and externally triggered disturbances in postural stability [32].
Balance can be classified into static and dynamic balance. Static balance refers to an
individuals ability to preserve a stable antigravity position while at rest by maintaining the
center of gravity within the available base of support. Dynamic balance involves automatic
postural responses to the disruption of the center of gravity position [28,29,34]. To maintain
balance in standing, the center of gravity must be kept upright within specific boundaries
of space, referred to as limits of stability. Thus limits of stability can be described as the
greatest distance a person can bend away from the base of support without changing
that base [20,35]. Limits of stability allow individuals to accomplish destabilizing effect of
gravity by performing small corrective sways in the anterior - posterior dimension as well
as laterally. A persons static postural alignment and the dynamic sway influence his or her
stability [29,34].
Balance requires proper information from sensory input, effective processing by the
Central Nervous System (CNS) and appropriate motor responses. Therefore, imbalance
can occur from lack of sensation, involvement of the CNS and decreased muscle strength
[29]. The CNS relies on information from three sensory systems: proprioception, visual and
vestibular. No single system supply all the information. Each system has different role in
maintaining balance [29,36]. To stay in an upright position, it is necessary that the central
nervous system receives and integrates the position of different body parts and their relation
with each other and the surroundings [6]. Muscle tone and muscular actions maintain
human upright balance. When balance is distrupted, the upright posture is arranged by
a series of postural reflexes that can be initiated by the afferent information from visual,
vestibular and somatosensory pathways [37-39].
Visual inputs maintain an individual information about physical surroundings correlative
to the position and movement of the head. Visual signals are particularly important when
proprioceptive inputs are untrustworthy [29]. The visual system not only takes part in
balance control on the basis of its unique property as a telereceptor (distance), but it also
maintains on-line feedback regarding body movements and postural sway. Vision decreases
postural sway, because the optic flow composed by head sway generates fairly automatic,
subconscious, postural corrections [40].
The vestibular system is appropriated in detecting angular (semicircular canals) and
linear (otoliths: utricule and saccule) movements of the head. This input is centrally handled
to control balance in at least three ways:
(a) Low-level reflexes such as vestibulo-spinal or vestibulo-ocular reflexes,
(b) Higher-order motor reactions interacting with voluntary motor control; and
(c) The generation of conscious sensations of head orientation and movement [40,41].
The sensory component of the vestibular system gauges the angular velocity and linear
acceleration of the head and identifies the position of the head relative to gravity. The
motor component however, uses motor pathways for postural stability and coordinated
movement [29]. The vestibulospinal reflex initiates a persons convenient body movements
to maintain an upright posture and to balance the head and trunk. The vestibulo-ocular

5
reflex, on the other hand, stabilizes vision during head and body motions, thus allowing
for proper dynamic vision. Vestibular system is dominant when a collision exists between
proprioceptive and visual cues for postural control [29,42].
Proprioception plays a major role in stabilising postural equilibrium during both quiet
stance and unexpected postural perturbations [43-45]. Proprioception inputs provide
information about the orientation of the body and body parts relative to each other and
the support surface. Information is received from joint and skin receptors, deep pressure
and muscle proprioception. Propriception cues are the dominant inputs for maintaining
balance when support surface is firm and fixed [29,36]. As with the vestibular system,
such input is able to control balance at multiple hierarchical CNS levels, particularly using
input from segments critically involved in postural control such as the cervical, ankle, and
plantar spinal afferents. Patients deprived of somatosensory input display greater and more
permanent postural dysfunction and disability than patients with peripheral vestibular
loss, even those with total bilateral vestibular loss [40].
Vestibular, proprioceptive, and visual inputs usually generate congruent postural
reactions, such that if a person standing upright is pushed forwards, head acceleration
(vestibularly mediated), soleus stretch (proprioceptive), and visual inputs will all demonstrate
forwards body motion and thus generate an integrated corrective postural response
backwards [40].
The cortex, in some way, plays a role in processing multisensory information and
modifying human balance. Moreover, it has been asserted that vestibular and somatosensory
input may be integrated within a distributed cortical network, including the temporal-
parietal cortex, supplementary motor area, and prefrontal cortex, in order to process input
related ego-motion and counter a loss of balance [46]. The information from the a variety of
sensory systems is transferred to the CNS and is integrated in several areas including the
vestibular nuclei and the cerebellum prior to the initiation of appropriate motor responses.
Prioritization of use of sensory information for use by the CNS is most likely based on the
availability of a special sensory modality, the task impended, and past experiences [30,47]. The
CNS then initiates the appropriate motor responses to maintain upright body posture [47].

Proprioceptive Contribution of Plantar Foot Sensation on Balance

Proprioception is defined as any postural, positional, or kinetic information provided to
the central nervous system by sensory receptors in muscles, tendons, joints, or skin [13].
There are three functions of proprioceptive system:
(1) The perception of limb movement is mediated by muscle spindle receptors, cutaneous
mechanoreceptors, and joint receptors;
(2) The perception of limb position is brought about by muscle spindle receptors and
cutaneous mechanoreceptors and
(3) the perception of force of muscular contraction is mediated by corollary discharges
and tendon organ receptors [48].
Some movements begin so rapidly that proprioceptive feedback is the only system
that helps planning before the movement begins and helps verifying the outcome after
the movement is completed [49]. With slower movements the proprioceptive system can
monitor and even corrects the movement as it occurs [50]. Especially during standing
balance, proprioceptive system trigger immediate rapid and precisely- tailored compensatory
muscular contractions reflexively in response to unexpected changes in external or internal
forces [2]. The proprioceptive receptors in the lower legs or feet are susceptible to ankle
rotation and can provide information about postural stability because most postural sway
occurs at the ankles [43]. The lower leg proprioceptive feedback is considered crucial for

6
human automatic postural control correcting responses [6,24]. However, this supposition is
not supported by Bloem et al., [51] that has shown that balance-correcting responses can
be stimulated in subjects whose lower leg proprioceptive feedback has been blocked. This
study suggests that lower leg proprioception is not required for initiating many balance
corrections [52]. Therefore, the role and significance of lower leg proprioception in balance-
correcting reactions remains unclear [6]. This leads us to the other parameters of the
somatosensory system.
The cerebral cortex receives proprioceptive data from the lower limbs almost merely by the
spinomedullary tract in the dorsolateral white column [2]. Depending on both, their location
within the body and their selectivity, the different kinds of receptors probably maintain
the brain with supplementary sensory information. A proprioceptive signal generates from
the ankle muscle which has been lengthened, may result form either a whole-body or
a supporting surface displacement [53]. Therefore, to emphasize appropriate postural
regulations, the central nerve system might compare the sensory information from the
various sources [53]. Signals from different resources interact with each other, depending
on the task [54].
Musculoskeletal receptors and vestibular system are considered full-time members of
the proprioceptive system, then skin receptors and the retina of the eye may be described
as part-time proprioceptors [2,43,53]. Primary role of the skin receptors is thought as
reacting to stimuli derived from the external environment, however, sometimes they provide
proprioceptive information about the musculoskeletal framework to the central nervous
system [2]. For example; during standing, afferent information from skin receptors in
plantar foot can be used by the proprioceptive centres of the brain to help clarify the posture
of the more proximal limb and axial joints [53]. Specific mechanoreceptors that have been
implicated in proprioception include SA type II cutaneous afferents that respond to planar
stretch of the skin and muscle spindle endings that respond to muscle stretch. Neither of
these receptors cause a coherent sensation when stimulated in isolation. This suggests that
spatial summation among various receptors is critical for the perception of position sense
[53]. Kavounoudias et al ., [24] demonstrated that plantar cutaneous afferents contribute
to the sensorial information required for human postural control. These authors suggested
that the plantar cutaneous information from the plantar mechanoreceptors contributes to
body position awareness. In addition, Billot et al., [55] investigated the cooling of plantar
sole mechanoreceptors through ice diving and its effects on balance control and lower leg
muscle activity, and concluded that a decrease of plantar sole sensitivity in healthy adults
led to a temporary increase in the CoP speed. These studies suggest that proprioceptive
inputs from the plantar sole conduce to balance control during normal quiet standing.
Somatosensory input from the lower extremities has long been recognized as an important
source of sensory information in controlling standing balance [56]. There are several groups
of receptors in the lower limb that may procure feedback related to stance and movement.
Proprioceptive data from muscle spindles in muscles from around the knee and ankle may
codify for the change in joint angle relative to trunk, while Golgi tendon organs may be liable
for force feedback about the positioning of the body, finally skin receptors in the plantar
foot are responsive to contact pressures [1]. The receptors involved in maintaining tactile
sensations to the central nervous system are Merkels cells, Pacinian corpuscles, Meissners
corpuscles, and Ruffini endings [6,7,10-12]. Since these cutaneous mechanoreceptors can
be found in the plantar foot, being the borderline between the body and the ground, they
might play an significant role in controlling upright stance. A change in upright position
is commonly related to an alteration in pressure under the feet [6]. Plantar cutaneous
afferents could potentially provide precious feedback to the balance control system leading
to the production of ankle torque, weight transfer between the legs, the proportion of limb
loading, and/or the nature of the support surface [57]. Feeling of pressure under the
feet, shear direction and normal direction to the skin during stance, might also be used to

7
initiate an internal estimate of the body Center-of-Mass (COM) location [57,58]. Sensorial
information from the plantar cutaneous receptors appears to be most important in the up
keep of AP postural control [59]. The small active postural reaction which observes with
skin stimulation alone likely represents a protection response to reduce pressure under the
forefoot when the skin indentation increased [37]. Such a reaction may normally occur,
for instance, when we are standing with the forefeet on rough stones and the heels on soft
grass. Yet, when body equilibrium becomes risked by some external stimulation, like with
the platform tilt in plantar sensation, the control of balance may alter from a weighting of the
sole protection mechanism by somatosensory exteroception (`somatosensory graviception`)
[37]. It was found that patients with chronic bilateral vestibular loss (Ps) can successfully
balance on a moveable platform in the absence of visual orientation signs at low tilt, unlike
at high frequencies [9]. This ability was refered to a `somatosensory graviception from
receptors in the feet, which complements vestibular graviception in Normal subjects (Ns)
[37]. However, Maurer et al., [37] investigated whether the input used for somatosensory
graviception stems from the aforesaid cutaneous receptors. Firstly, it was evaluated the
postural responses to mechanical stimulation of the plantar soles, using frequencies in
the range of natural postural sway ( <0.2 Hz). Secondly, it was evaluated the effect of this
plantar stimulation on postural reactions to platform tilts. Finally, it was concluded that the
plantar skin receptors are primarily involved in exteroceptive tasks, like the evaluation of
the the support surface when standing, rather than contributing to the continuous control
of COM and COP under the constraint to provide body equilibrium [37].
Tactile afferents from the plantar foot provide the information about the body position
to the CNS [53]. Moreover, plantar inputs may be co-worked with ankle proprioceptive
inputs for supplemental postural function [60]. During standing, afferent information from
plantar foot receptors can be used by proprioceptive centres of the brain to help declaring
the posture of the more proximal limb and axial joints [2,53]. Therefore, cutaneal signals are
thought to play a double role. These are to identify body orientation in space and to specify
the support surface on which the feet are resting [61]. The large sensory nerve fibers, or
the A fibers, are mostly responsible for the innervation of muscle spindles and the Golgi
tendon organs. Smaller fibers, the group of A fibers, are responsible for the innervation
of the cutaneous receptors (e.g. Merkels cells, Pacinian corpuscles, Meissners corpuscles,
and Ruffini endings in the plantar foot). However, muscle spindles, Ruffinis joint receptors
and Pacinian joint receptors are also innervated by A, which implies that the A fibers
are both responsible for tactile and proprioceptive sensation [6,62]. The A fibers seem
to convey more significant information for stance control than A fibers. Therefore, large
fibers are less significant in postural control than the small fibers [6]. Additionally, when
the mechanoreceptors are compared in themselves, Merkels cells and Ruffini endings (slow
adapting receptors) are more important in standing balance control than the Meissners
and Pacinian corpuscles (fasting-adapting receptors) [6,62-64]. This idea was supported
by Perry et al., suggesting that, Merkels cells and Ruffini endings, based on their slow-
adapting properties, play a key role in quiet stance [65].
Plantar foot sensitivity is correlated with plantar pressure distribution [66]. Skin
mechanoreceptors are very responsive to mechanical vibration, especially the slowly adaptive
receptors which are able to code every pressure change initiated on their receptive areas [10].
Varying the pressure under the supporting points of the soles changes postural responses
[37]. Therefore appliying vibration under a certain plantar area probably stimulates a local
pressure increase, as when the body is actually bent in the direction of this area [53]. In
healthy individuals, regional plantar pressures modify in response to alterations in the
sensory input on the plantar foot during walking and standing [66]. However, neuropathy
patients with decreased cutaneous sensation have different plantar pressure distributions
compared to healthy individuals [67,68]. This suggests that decreased plantar pressure
sensitivity contributes to postural control deficiencies in people with cutaneal sensation
loss [63]. Studies investigated the effect of acutely reduced sensation on the plantar

8
pressure distribution in healthy people by appliying insensitivity on the whole, fore, or rear
foot [53,63,66]. Nurse et al., reduced the sensitivity on whole, fore and rear plantar foot
respectively by ice immersion. The general tendency in this study was load relaying away
from the insensitive to the sensitive area during walking [66]. Zhang et al., examine the
effects of chronic sensory loss on plantar pressure distribution in walking and standing
and reported that plantar pressure distribution changes significantly only in standing as
a result of insensitivity [63]. Additionally, after proprioceptive stimulation the body tilted
forwards and backwards in the case of tactile stimulation. Kavounoudias et al., showed
that, as for vibratory stimulation, the body tilted backwards after stimulaton of the forefoot
plantar zones, forwards in the case of co-stimulation of the two heels, and laterally after the
one plantar foot stimulation [53].
The postural function of cutaneous afferents from the plantar sole has been studied
in many researches [6,20,34,37,58,59,69]. Clinically distal sensory neuropathy in the
feet is known to disrupt postural control [6]. Different studies tried to confirm the this
suggestion using different experimental designs to influence the tactile afferent information
[6,24,58]. In these experiments, postural stability decreased by diminishing sensibility by
cooling the plantar cutaneous mechanoreceptors, anesthetizing the receptors, or changing
the characteristics of the supporting surface on which the subject is standing [6,58,70].
Additionally, cooling or anaesthetising the plantar soles of upright standing human subjects
leads to increase in postural sway [37,41,59,69,71]. Also, when vibration is applied to
the main foot-supporting regions of a standing subject, involuntary whole-body tilt was
stimulated as a reaction to this vibration [24,53]. Roll et al ., [60] investigated whether
the tactile information from the main supporting areas of the foot are used by the brain
for perceptual intentions, so body posture awareness and body representation in space.
Varied patterns of tactile stimulation were applied to one or both soles of standing with
no movement and blindfolded subjects by a 60 micro-vibrator tactile matrix set in a force
platform. The perceptual effects of the stimulation were evaluated through a 3D joystick
handled by the subjects . It was concluded that plantar foot input lends to the coding
and the spatial presentation of body posture [60]. The contribution of plantar cutaneous
afferents to postural control is largely evidenced by these protocols. However, the rate of
this contribution remains unclear. There are also studies advocating the opposite opinion
[6,69]. For example, McKeon et al., assessed the effect of diminished plantar cutaneous
sensation induced by cooling on postural control during double- and single-limb quiet
standing, and concluded that no significant differences for plantar hypoesthesia was seen
in single-limb stance [69]. Also, Kars et al., [6] wanted to identify and review publications
describing the impact of reduced somatosensation on balance, and concluded that the
effect of plantar sensation reduction on postural control is unclear [6]. Therefore, postural
function of cutaneous afferents from the plantar sole was still controversially discussed.
Plantar cutaneous mechanoreceptors contribute postural control by a reflex modulation.
Foot skin receptors may be functionally involved inexteroceptive and proprioceptive
processing by informing the brain about body parts and quality of support surface [60].
Populations of cutaneous and muscle afferents can maintain short-latency facilitation of
motoneuron pools [5]. Postural reflexes in the leg muscles can be revealed in subjects
standing on a movable platform that is sensitive to maneuvers such as a fast toes-up tilt
[72]. Based on the delay in time from the stimulus to the muscle response, these reflexes
have been classified as Short Latency (SL), Medium Latency (ML) and Long Latency (LL )
[72,73]. Evidence has shown that these responses in the leg muscles are less associated with
the visual and vestibular afferents than the somatosensory pathways welded from the foot
[70]. Reflex modulation of lower limb muscles by cutaneous afferents had been suggested by
Sherrington [74]. In the foot, the reflexes are likely to be associated with information related
to foot contact (FA I mechanoreceptors) and the provided contact of the foot on a support
(SA I mechanoreceptors ) [5]. That may aids in signaling different phases of the gait cycle
and the reflex control of posture [5]. The most commonly observed reflex couplings (55% of

9
all reflexes) were explained by the FA I mechanoreceptors. These afferents were innervated
by mechanical stimulation across their receptive areas which resulted in periodic bursts
of afferent activity, and subsequent cyclic reflex modulation at the frequecy of the periodic
activation [5]. Fallon et al ., [5] recorded fifty- three low threshold mechanoreceptors in
the glabrous skin of the foot via microelectrodes inserted percutaneously into the tibial
nerve of healthy human subjects. Finally it was found that reflex modulation of ongoing
whole muscle electromyography was observed for each of the four classes of low threshold
cutaneous mechanoreceptors (Fast adapted Type I, Fast adapted type II, Slow adapted type
I, Slow adapted type II). The activity of individual low- threshold mechanoreceptors in the
glabrous skin of the foot had been shown to cause a obvious reflex modulation in ankle
muscles. It was also indicated that all classes of tactile afferent were exhibit some form of
reflex coupling [5].
In the absence of any of the somatosensory balance parameters, compensation develop
by other systems. Stal et al., [75] investigated the significance of information from plantar
cutaneous mechanoreceptors in postural control and whether postural control could
compensate for reduced cutaneous information by adaptation. It was suggested that
somatosensory input from mechanoreceptors in the plantar foots contribute significantly in
maintaining postural control, but the sensory loss could be compensated for [75]. Maurer et
al ., [61] investigated the changes of human posture control of upright stance which occur
when vestibular cues (VEST) are absent and visual and somatosensory orientation cues
(VIS, SOM) are removed. Postural responses to sinusoidal tilts of a motion platform in the
sagittal plane were evaluated in Normal subjects (Ns) and patients with bilateral vestibular
loss (Ps). It was found that absence of VEST (Ps, visual reference) and removal of VIS (Ns,
no visual reference) had little effect on stabilization of upright body posture in space. In the
absence of both VEST and VIS (Ps, no visual reference) somatosensory graviception still
maintained some information on body orientation in space at 0.05 and 0.1 Hz. However,
at the higher frequencies vestibular loss qualitatively changed their response; they then
tended to actively fix their bodies with respect to the motion platform [61].
In conclusion, although tactile sensitivity can be considered an exteroceptive modality,
it could be said that for a proprioceptive function of tactile inputs from the plantar foot
directly contribute to body representation. Tactile and proprioceptive afferents from soles
and ankle muscles could subserve complementary functions for postural purposes. In case
of proprioceptive and vestibular sensory input reduction, tactile senses would be responsible
for perceiving body segments position. As a result of insensitivity of plantar foot, plantar
pressure distribution, body sway and COP are significantly changed especially in standing.
In addition, there is a reflex modulation of lower limb muscles by cutaneous afferents. So
every tactile stimulation from plantar foot can cause a reflex stimulus to ankle muscle
spindles, by which proprioceptive information is conveyed to CNS.

References
1. Kennedy PM, Inglis JT (2002) Distribution and behaviour of glabrous cutaneous receptors in the human foot
sole. J Physiol 538: 995-1002.
2. Stillman BC (2002) Making sense of proprioception: The meaning of proprioception, kinaesthesia and related
terms. Physiotherapy 88: 667-676.
3. Patel M, Magnusson M, Kristinsdottir E, Fransson PA (2009) The contribution of mechanoreceptive sensation
on stability and adaptation in the young and elderly. Eur J Appl Physiol 105: 167-173.
4. Knikou M (2010) Plantar cutaneous afferents normalize the reflex modulation patterns during stepping in
chronic human spinal cord injury. J Neurophysiol 103: 1304-1314.
5. Fallon JB, Bent LR, McNulty PA, Macefield VG (2005) Evidence for strong synaptic coupling between single
tactile afferents from the sole of the foot and motoneurons supplying leg muscles. J Neurophysiol 94: 3795-
3804.

10
6. Kars HJ, Hijmans JM, Geertzen JH, Zijlstra W (2009) The effect of reduced somatosensation on standing
balance: a systematic review. J Diabetes Sci Technol 3: 931-943.
7. Bolanowski S (2002) Somatosensory coding. In: Roberts D (ed.). Signals and perception: The fundementals
of human sensation. Palgrave Macmillan, Oxford, Pg: 233-245.
8. Greenspan JD, Bolanowski SJ (1996) The psychophysics of tactile perception and its peripheral physiological
basis. In: Kruger L (ed.). Handbook of perception and cognition, 7: Pain and touch. Academic Press, San
Diego.
9. Iggo A (1973) Handbook of sensory physiology, II Somatosensory system. Springer- Verlag, Berlin.
10. Abraira VE, Ginty DD (2013) The sensory neurons of touch. Neuron 79: 618-639.
11. Lundy-Eckman L (2002) Neuroscience: Fundamentals of rehabilitation. WB Saunders Co, Philadelphia.
12. Waite PME (1999) Sensory System. In: Bray JJ, Patricia A Cragg, Macknight ADC, Mills RG, Taylor DW (eds.).
Human physiology. Blackwell Science, Oxford, Pg: 128-143.
13. Rowin R, Meriggioli MN (2007) Proprioception, touch and vibratory sensation. In: Goetz CG (ed.). Textbook of
Clinical Neurology. Saunders, Philadelphia, Pg: 343-361.
14. Johansson RS, Vallbo AB (1979) Tactile sensibility in the human hand: relative and absolute densities of four
types of mechanoreceptive units in glabrous skin. J Physiol 286: 283-300.
15. Frost LR, Bijman M, Strzalkowski ND, Bent LR, Brown SH (2015) Deficits in foot skin sensation are related
to alterations in balance control in chronic low back patients experiencing clinical signs of lumbar nerve root
impingement. Gait Posture 41: 923-928.
16. Simoneau GG, Ulbrecht JS, Derr JA, Becker MB, Cavanagh PR (1994) Postural instability in patients with
diabetic sensory neuropathy. Diabetes Care 17: 1411-1421.
17. Citaker S, Gunduz AG, Guclu MB, Nazliel B, Irkec C, et al. (2011) Relationship between foot sensation and
standing balance in patients with multiple sclerosis. Gait Posture 34: 275-278.
18. Strzalkowski NDJ, Lowrey CR, Perry SD, Williams DR, Wood SJ et al. (2015) Selective weighting of cutaneous
receptor feedback and associated balance impairments following short duration space flight. Neurosci Lett
592: 94-98.
19. Corriveau H, Prince F, Hbert R, Rache M, Tessier D, et al. (2000) Evaluation of postural stability in elderly
with diabetic neuropathy. Diabetes Care 23: 1187-1191.
20. Lafond D, Corriveau H, Prince F (2004) Postural control mechanisms during quiet standing in patients with
diabetic sensory neuropathy. Diabetes Care 27: 173-178.
21. Johansson RS (1978) Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive
units in the glabrous skin area. J Physiol 281: 101-125.
22. Johansson RS, Vallbo AB (1979) Tactile sensibility in the human hand: relative and absolute densities of four
types of mechanoreceptive units in glabrous skin. J Physiol 286: 283-300.
23. Johansson RS, Vallbo AB (1980) Spatial properties of the population of mechanoreceptive units in the glabrous
skin of the human hand. Brain Res 184: 353-366.
24. Kavounoudias A, Roll R, Roll JP (1998) The plantar sole is a dynamometric map for human balance control.
Neuroreport 9: 3247-3252.
25. Burgees PR, Perl ER (1973) Cutaneous mechanoreceptors and nociceptors. In: Iggo A, (ed.). Handbook of
Sensory Physiology. Springer Verlag, Berlin, Pg: 29-78.
26. Birder LA, Perl ER (1994) Cutaneous sensory receptors. J Clin Neurophysiol 11: 534-552.
27. Brodal A (1981) Neurological Anatomy in Relation to Clinical Medicine, (3rd edition). Oxford University Press,
Oxford.
28. Nashner L (1994) Evaluation of postural stability, movement and control. In: Hasson S (ed.). Clinical exercise
physiology. Mosby, St. Louis, Pg: 1999-1234.
29. Wallace B (2001) Balance Training. In: Bandy WD, Sanders B (eds.). Therapeutic Exercise: Techniques for
Intervention, Lippincott Williams & Wilkins, Philadelphia, Pg: 239-263.

11
30. Wrisley DM, Kauffman TL (2014) Balance testing and training. In: Kauffman TL, Scott, Barr, Moran, (eds.). A
Comprehensive Guide to Geriatric Rehabilitation (3rd edition). Churchill Livingstone Elsevier,Edinburgh, Pg:
433-438.
31. Shumway- Cook A, McCollum G (1993) Assessment and treatment of balance disorders. In: Montgomery PC,
Connolly BH, (eds.). Motor control and physical therapy. Chattanooga Group, Hixson, Pg. 123-138.
32. Horak FB (2006) Postural orientation and equilibrium: what do we need to know about neural control of balance
to prevent falls? Age Ageing 35 Suppl 2: ii7-7ii11.
33. Massion J (1994) Postural control system. Curr Opin Neurobiol 4: 877-887.
34. Nashner L (1990) Sensory, neuromuscular and biomechanical contributions to human balance. In: Duncan
PW, (ed.). Balance: proceedings of APTA forum. APTA, Alexandria, Pg: 33-38.
35. McCollum G, Leen TK (1989) Form and exploration of mechanical stability limits in erect stance. J Mot Behav
21: 225-244.
36. Hobeika CP (1999) Equilibrium and balance in the elderly. Ear Nose Throat J 78: 558-562, 565-6.
37. Maurer C, Mergner T, Bolha B, Hlavacka F (2001) Human balance control during cutaneous stimulation of the
plantar soles. Neurosci Lett 302: 45-48.
38. Inglis JT, Horak FB, Shupert CL, Jones-Rycewicz C (1994) The importance of somatosensory information in
triggering and scaling automatic postural responses in humans. Exp Brain Res 101: 159-164.
39. Fitzpatrick R, Rogers DK, McCloskey DI (1994) Stable human standing with lower-limb muscle afferents
providing the only sensory input. J Physiol 480 : 395-403.
40. Bronstein AM, Pavlou M (2013) Balance. Handb Clin Neurol 110: 189-208.
41. Mnchau A, Bronstein AM (2001) Role of the vestibular system in the pathophysiology of spasmodic torticollis.
J Neurol Neurosurg Psychiatry 71: 285-288.
42. Horak FB (2010) Postural compensation for vestibular loss and implications for rehabilitation. Restor Neurol
Neurosci 28: 57-68.
43. Fitzpatrick R, McCloskey DI (1994) Proprioceptive, visual and vestibular thresholds for the perception of sway
during standing in humans. J Physiol 478 : 173-186.
44. Nardone A, Grasso M, Schieppati M (2006) Balance control in peripheral neuropathy: are patients equally
unstable under static and dynamic conditions? Gait Posture 23: 364-373.
45. Peterka RJ, Benolken MS (1995) Role of somatosensory and vestibular cues in attenuating visually induced
human postural sway. Exp Brain Res 105: 101-110.
46. Slobounov SM, Newell KM (2009) Balance and Posture Control In: Squire LR, (ed.). Encyclopedia of
Neuroscience. Academic Press, California, Pg: 31-35.
47. Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88: 1097-1118.
48. Jones LA (1986) Perception of force and weight: theory and research. Psychol Bull 100: 29-42.
49. McCloskey DI, Gandevia SC (1993) Aspects of proprioception. In: Gandevia SC, Burke D, Anthony M, (eds.).
Science and Practice in Clinical Neurology, Cambridge University Press, Cambridge, Pg: 3-19.
50. Hasan Z, Stuart DG (1988) Animal solutions to problems of movement control: the role of proprioceptors. Annu
Rev Neurosci 11: 199-223.
51. Bloem BR, Allum JH, Carpenter MG, Honegger F (2000) Is lower leg proprioception essential for triggering
human automatic postural responses? Exp Brain Res 130: 375-391.
52. Bloem BR, Allum JH, Carpenter MG, Verschuuren JJ, Honegger F (2002) Triggering of balance corrections
and compensatory strategies in a patient with total leg proprioceptive loss. Exp Brain Res 142: 91-107.
53. Kavounoudias A, Roll R, Roll JP (2001) Foot sole and ankle muscle inputs contribute jointly to human erect
posture regulation. J Physiol 532: 869-878.
54. Van Deursen RW, Simoneau GG (1999) Foot and ankle sensory neuropathy, proprioception, and postural
stability. J Orthop Sports Phys Ther 29: 718-726.

12
55. Billot M, Handrigan GA, Simoneau M, Corbeil P, Teasdale N (2013) Short term alteration of balance control
after a reduction of plantar mechanoreceptor sensation through cooling. Neurosci Lett 535: 40-44.
56. Allum JH, Bloem BR, Carpenter MG, Hulliger M, Hadders-Algra M (1998) Proprioceptive control of posture: a
review of new concepts. Gait Posture 8: 214-242.
57. Morasso PG, Schieppati M (1999) Can muscle stiffness alone stabilize upright standing? J Neurophysiol 82:
1622-1626.
58. Meyer PF, Oddsson LI, De Luca CJ (2004) The role of plantar cutaneous sensation in unperturbed stance.
Exp Brain Res 156: 505-512.
59. McKeon PO, Hertel J (2007) Plantar hypoesthesia alters time-to-boundary measures of postural control.
Somatosens Mot Res 24: 171-177.
60. Roll R, Kavounoudias A, Roll JP (2002) Cutaneous afferents from human plantar sole contribute to body
posture awareness. Neuroreport 13: 1957-1961.
61. Maurer C, Mergner T, Bolha B, Hlavacka F (2000) Vestibular, visual, and somatosensory contributions to
human control of upright stance. Neurosci Lett 281: 99-102.
62. Shaffer SW, Harrison AL (2007) Aging of the somatosensory system: a translational perspective. Phys Ther
87: 193-207.
63. Zhang S, Li L (2013) The differential effects of foot sole sensory on plantar pressure distribution between
balance and gait. Gait Posture 37: 532-535.
64. Nardone A, Tarantola J, Miscio G, Pisano F, Schenone A, et al. (2000) Loss of large-diameter spindle afferent
fibres is not detrimental to the control of body sway during upright stance: evidence from neuropathy. Exp Brain
Res 135: 155-162.
65. Perry SD, McIlroy WE, Maki BE (2000) The role of plantar cutaneous mechanoreceptors in the control of
compensatory stepping reactions evoked by unpredictable, multi-directional perturbation. Brain Res 877: 401-
406.
66. Nurse MA, Nigg BM (2001) The effect of changes in foot sensation on plantar pressure and muscle activity.
Clin Biomech (Bristol, Avon) 16: 719-727.
67. Chen H, Nigg BM, Hulliger M, de Koning J (1995) Influence of sensory input on plantar pressure distribution.
Clin Biomech (Bristol, Avon) 10: 271-274.
68. Caselli A, Pham H, Giurini JM, Armstrong DG, Veves A (2002) The forefoot-to-rearfoot plantar pressure ratio is
increased in severe diabetic neuropathy and can predict foot ulceration. Diabetes Care 25: 1066-1071.
69. McKeon PO, Hertel J (2007) Diminished plantar cutaneous sensation and postural control. Percept Mot Skills
104: 56-66.
70. Wu G, Chiang JH (1997) The significance of somatosensory stimulations to the human foot in the control of
postural reflexes. Exp Brain Res 114: 163-169.
71. Magnusson M, Enbom H, Johansson R, Pyykk I (1990) Significance of pressor input from the human feet in
anterior-posterior postural control. The effect of hypothermia on vibration-induced body-sway. Acta Otolaryngol
110: 182-188.
72. Timmann D, Belting C, Schwarz M, Diener HC (1994) Influence of visual and somatosensory input on leg EMG
responses in dynamic posturography in normals. Electroencephalogr Clin Neurophysiol 93: 7-14.
73. Beckley DJ, Bloem BR, Remler MP, Roos RA, Van Dijk JG (1991) Long latency postural responses are
functionally modified by cognitive set. Electroencephalogr Clin Neurophysiol 81: 353-358.
74. Sherrington CS (1910) Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing.
J Physiol 40: 28-121.
75. Stl F, Fransson PA, Magnusson M, Karlberg M (2003) Effects of hypothermic anesthesia of the feet on
vibration-induced body sway and adaptation. J Vestib Res 13: 39-52.

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