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Proprioception: The Forgotten
Sixth Sense
Chapter: Spine and Proprioception
Edited by: Defne Kaya
Published Date: May, 2015
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Spine and Proprioception
Mehmet Gürhan Karakaya* and İlkim Çıtak Karakaya
Associate Professor, Muğla Sıtkı Koçman University, Muğla School of Health,
Department of Physiotherapy and Rehabilitation, Turkey
*Corresponding author: DMehmet Gürhan Karakaya, Associate Professor, Muğla
Sıtkı Koçman University, Muğla School of Health, Department of Physiotherapy and
Rehabilitation, Turkey, E-mail: [email protected]
Abstract
Proprioception is an important component of the sensory-motor system, and it can be
defined as sense of movement (kinesthesia), position and tension of extremities or trunk,
which is perceived at both conscious and subconscious levels. Decreased proprioception of
the trunk can lead to a delay on the reaction-time, and disorders in postural control and
stability. In order to provide postural control, afferent inputs generated by the multisensors
(visual, labyrinth, proprioceptive, cutaneous and graviceptive, etc.) which perceive body
schema (geometry, weight, verticality, etc.) are processed by the postural network, and
are used for neuromuscular control. During movement, consistently changing positions of
head, trunk, and extremities are processed easily by these systems and the adaptation of
body to these position changes is provided. In this chapter, the relations of spinal column
structures with spinal proprioception will be addressed.
Keywords:
Trunk
Neuromuscular Control; Postural Control; Proprioception; Spinal Stability;
Proprioception
Proprioception is an important component of the sensory-motor system, and it can be
defined as sense of movement (kinesthesia), position and tension of extremities or trunk,
which is perceived at both conscious and subconscious levels. Charles Bell was first to identify
the fundamental anatomical basis for sense/perception and movement: ‘Between the brain
and the muscles there is a circle of nerves; one nerve (ventral roots) conveys the influence
from the brain to the muscle, another (dorsal roots) gives the sense of the condition of the
muscle to the brain’. Bell included within this muscular sense the senses of position and
movement, and other senses evoked by muscle contractions. Sense of tension is to perceive
the force, which muscles create on joints. Whereas sense of position is to describe different
body parts and to perceive their positions, kinesthesia is to perceive the amount of the
movement. Proprioception is a multi-component sensorial system. Proprioceptive afferent
1
information is obtained from skin, ligament, facet joint, intervertebral disc, intramuscular
peripheral receptors. The information from these receptors is transmitted from medulla
spinalis to cortex via important sensory afferent pathways. Transmitted afferent information
is processed for neuromuscular control by Central Nervous System (CNS), and is used for
providing dynamic joint stability [1-9].
Proprioceptors of the human body are usually grouped in three main topics:
A. Fascial/joint proprioceptors
B. Muscular proprioceptors
C. Graviceptors
A. Fascial/joint proprioceptors These are mechanoreceptors which exist in joint capsules and around deep muscular
fascia. They produce information about the static position and dynamic movement of the
joint.
When the position of joint changes, the soft tissues around the joint are compressed
on one side of the joint and stretched on the other side. The mechanical forces created by
the tension and compression, cause a deformation over joint proprioceptors. The stimulus
generated by this mechanical deformation causes the joint proprioceptors to fire, sending
signals into the CNS.
Joint mechanoreceptors (proprioceptors) can be divided into 3 groups:
Pacini's Corpuscules
•Adapt quickly to
mechanichal force.
•Only sensitive to and
stimulated by changes in
position (i.e., movement)
•Are responsible for
kinesthetic motion sense
Ruffini's Endings
•Adapt slowly to
mechanichal force.
•Sensitive to and stimulated
by changes in position (i.e.,
movement) and the static
position of the joint
İnterstitial Myofacial
Receptors
•Mechanoreceptors located
in and around the capsules
of joints.
•Actually the most
numerous receptor found
within deep dense fascia.
•They are small receptors.
•Some are fast adapting and
some are slow adapting.
•To be involved in pain
reception and
proprioception.
B. Muscle receptors Muscle spindles: They are mechanoreceptors which are sensitive to the tension of
muscle.
• Intrafusal fibers have both afferent and efferent nerve fibers, and also nerve endings
connected to these fibers. Whereas efferent interconnections are on the Polar Regions
which have a contractile property, afferent interconnections are more located at the
center of muscle fibers.
This fiber and its endings can be indicated as the following:
2
Group Ia
Group II
Afferent
Also known as primary fibers,
Connected to annulospiral (dynamic) endings,
Sensitive to the velocity of mechanical change in muscle.
Also known as secondary fibers,
Connected to flower spray (static) endings,
Sensitive to amplitude of mechanical change in muscle.
Efferent
Gamma
Comes to the contractile polar regions,
It is connected to the relevant motor-end-plate
•
Extrafusal fibers are components of muscle spindles with contractile property.
Alfpha
Efferent
Comes to the contractile polar regions,
It is connected to the relevant motor-end-plate
Golgi tendon organs: They are mechanoreceptors located in the tendon of muscle, and are sensitive
to the pulling force generated by the contractile structure, during contraction.
Group Ib
•
Afferent
It is located in the musculotendinous junction.
It is connected to the muscle fibers.
It perceives the pulling force which the contraction creates on the
tendon.
Extrafusal fibers are components of muscle spindles with contractile property.
Golgi tendon organs: They are mechanoreceptors located in the tendon of muscle, and
are sensitive to the pulling force generated by the contractile structure, during contraction.
C. Graviceptors Graviceptors are the receptors which perceive the changes of the body with respect to
the gravity line.
There are two groups of graviceptors: vestibular (otolith) and extravestibular.
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The aim of proprioceptive postural chain is not only to decide the position of body
segments but also to provide postural orientation of the body against outer environment/
world. Graviceptors located at trunk (around kidney) and head (otoliths) are important
receptors for this orientation. It is said that graviceptors responsible for perceiving static
longitudinal loads are mostly located at head and truck rather than at extremity and skin
[7,10-13].
McLain and Raiszadeh (1995), Freeman and Wyke (1967) have categorized the above
mentioned mechanoreceptors into four types according to their properties such as location,
functional characteristics, etc. [12,14] (Table 1).
Type
Morphological features
Location
Probable functional Other eponymous or
characteristics
descriptive designations
Type 1
Globular receptors. Round,
oval, or "bean shaped", thinly
encapsulated, usually found in
clusters.
Found in fibrous capsule of
joint, and in peri-articular
ligaments and tendons. Usually
in superficial layers of dense
connective tissue.
Mechanoreceptor.
(Slowly adapting,
low threshold
afferent ending).
Ruffini ending. GolgiMazzoni ending. Meissner
corpuscle. Basket or spraytype ending.
Type II
Found in deeper layers of
Cylindrical corpuscles with thick fibrous capsule, at junctions of
laminated encapsulations, and fibrous tissue and fat, and in fat
central axon core. Parent axon pads. Often accompanied by
may be bifid or trifid, entering at vascular leash. Oriented with
one terminal of the cylinder.
connective tissue fibers in dense
capsule or ligament.
Mechanoreceptor.
(Rapidly adapting,
low threshold
afferent ending).
Pacinian corpuscle,
Vater-Pacinian corpuscle.
Modified Pacinian
corpuscle. Paciniform
corpuscle. Meissner
corpuscle. Golgi-Mazzoni
body. Bulbous corpuscle.
Club-like ending.
Type III
Fusiform corpuscles with a thin
capsule surrounding a densely
arborizing nerve terminal. Fine
neuritis form meshwork visible at
higher magnification.
Found in ligaments and
tendons, as well as dense
fibrous connective tissue of joint
capsule.
Mechanoreceptor.
(Very slowly
adapting, high
threshold afferent).
Golgi ending, GolgiMazzoni corpuscle.
Type IV
Unmyelinated free nerve
endings and unencapsulated
plexuses.
Found in all peri-articular and
intra-articular tissues except for
cartilage.
Nociceptor (Nonadapting).
Table 1: Types of Graviceptors.
The communication between different components of the proprioceptive system is
provided by the central afferents conducted by the dorsal column, medial leminiscus,
and spinocerebellar pathways and by large-diameter, myelinated and fast-conducting
peripheral cutaneous and muscle afferents. Afferent pathways make collateral connections
at different levels until they reach to primary somatosensorial cortex. The first connection is
at the medulla spinalis level. Dendrites and axons of the peripheral neurons enter medulla
spinalis through dorsal root ganglions and connect to the nucleus cuneatous and nucleus
gracilis. Second connection is made by the axons extending from medulla spinalis to the
Ventral Posterolateral (VPL) nucleus of thalamus over brain stem. These axons form the
third connection by terminating in the primary somatosensory cortex [15].
Spinal Column Structures and Proprioception
The neuromuscular control of spinal column is provided by three important
structures. These are: vertebrae and ligaments (spinal ligaments, annular fibers
of intervertebral discs and facet capsule fibers) which provide passive support;
muscular system which provides dynamic support and; central nervous system
which conducts neuromuscular control. Vertebral column has two functions:
structural and transducer (mechanical power). The structural function provides
stiffness to the spine. Its function as a transducer is to transfer the required afferent
4
information into neuromuscular control unit via numerous mechanoreceptors
(located in intervertebral disc annular fibers, facet joint capsules and spinal column
ligaments) in order to arrange functions such as spinal posture, movement of the
vertebrae and carrying spinal loads. Neuromuscular control unit, which processes
this transmission, provides spinal stability via muscles [16-18].
The mechanosensitive afferent receptors located in intervertebral disc joints of the spinal
column, vertebral facet joints, spinal ligaments and spinal muscles are the structures
responsible for proprioception [19].
Intervertebral disc joint and proprioception
Intervertebral disc joint is composed of 3 morphologically different anatomic regions:
a. Nucleus pulposus: Nucleus Pulposus (NP), which is in the center of the intervertebral
disc, contains a great deal of proteoglycan. Proteoglicans, one of the constituents of the
cartilage tissue are hydrophilic molecules regulating fluid balance of the nucleus and
contain glycosaminoglycans such as sulphate, dermatan sulphate, keratan sulphate.
Nucleus pulposus is composed of type II collagen fibers in an irregular network structure
carries a constant negative load and produces an osmotic swelling pressure.
b. Annulus fibrosus: It is composed of 10-20 concentric rings of fibrous materials and
surrounds nucleus pulposus.
c. Vertebral endplate: It is a structure composed of both hyaline articular cartilage and
fibrocartilage and it lines the surface of the vertebral body. There are two endplates (inferior
and superior) in each intervertebral disc joint [7,20,21].
During the fetal period, nerves on superficial intervertebral disc surface are in forms
of free nerve endings. As the fetus grows, these free nerve endings increase in number.
Different types of receptors begin to develop in the postpartum period, and reach their latest
form in adulthood. Receptors in the intervertebral discs do not have a certain anatomic
location, and their distribution also change along with age. During the development period
following birth, receptors located on the anterior region of annulus plate start to decline
significantly. In adult individuals, free nerve endings are mostly located on the lateral region
of the annulus plate [22,23].
In studies about innervations of the intervertebral disc, it is indicated that
mechanoreceptors located in posterior and anterior longitudinal ligaments in addition to
the ones on the external part of the annulus fibrosus are the proprioceptive structures
responsible for creating sense of movement and posture. Therefore, proprioceptive input
is negatively affected after intervertebral disc surgeries due to loss of tissue in both
annular fibers and longitudinal ligaments, which are among the most important parts of
proprioceptive structure [19].
There are numerous proprioceptive nerve endings in the external part of a healthy
intervertebral disc. These are the branches of sinuvertebral nerve, the ventral rami
communicantes and gray rami communicantes nerves. Sinuvertebral nerve located in
each intervertebral disc space is a meningeal branch of the spinal nerve. This nerve
leaves the dorsal root ganglion of the spinal nerve and enters into the intervertebral
space through the nerve foramina. Then, it separates into thin efferent and thick
afferent branches. According to the animal studies, many afferent fibers connect to
sinuvertebral nerve through ramie communicantes from superior and inferior dorsal root
ganglia. In addition, the Anterior Longitudinal Ligament (ALL) gets also branches from
the dorsal root ganglion. Posterior longitudinal ligament is innervated by nociceptive
afferent branches of the sinuvertebral nerve. These nerves innervate the external layers
5
of the annulus fibrosus. Some of the intervertebral disc nerves have also glial support
or schwann cells [23].
The morphology of the mechanoreceptors located in the outer 2 or 3 lamels of human
intervertebral disc annulus fibrosus in addition to the nociceptive nerve fibers shows some
similarities to Pacini’s corpuscles, Ruffini’s endings and often Golgi tendon organs. Sensory
fibers located in intervertebral disc arise from neurons located in Dorsal Root Ganglia (DRG).
These neurons can be classified according to the neuronal size, ultrastructural features (large
pale, small dark and intermediate), neuropeptide or neurotransmitter content, cytoskeleton
composition, cytosolic proteins, ion channel expression or growth factor dependence. Each
type of DRG neurons makes different endings in the spinal cord and the target organs. In
addition, these neurons transfer different types of afferent information to CNS according to
their characteristic features.
According to the current knowledge;
• Large-diameter DRG neurons are proprioceptors, and innervate sensory organs in the
muscles and joints.
• Medium diameter neurons innervate peripheral mechanoreceptors.
• Small diameter neurons innervate different types of nociceptors. Intervertebral dics are
innervated primarily by small-diameter DRG neurons [24].
Spinal viscoelastic structures consisting of intervertebral disc, capsule and ligaments
are considerably important in terms of performing sensorial and motor functions. Afferents
capable of monitoring proprioceptive and kinesthetic information exist abundantly within
these structures.
Holm et al., (2001), in a study on 80 domestic pigs, have evaluated the effect of
mechanical elongation applied to the joint capsule, and also the effect of electrical
stimulation applied to the intervertebral disc, zygapophyseal joint capsule, the annulus
fibrosis, sacroiliac joint and the joint capsule membrane, on reflex muscle responses.
As electrical stimulation protocol, bipolar electrodes were unilaterally implanted under
general anesthesia on the L1-L2 intervertebral disc, zygapophyseal joint capsule and the
outer peripheral fibers of annulus fibrosis. In addition, direct stimulation was applied
bilaterally to the ventral aspect of sacroiliac joint and the joint capsule membrane through
lateral retroperitoneal hypodermic needle electrode. It was inflated by injecting fluid into
the joint in order to stimulate the tension of joint capsule membrane mechanically.
The authors have measured reflex Motor Unit Action Potential (MUAP) responses of
multifidus, longissimus, gluteus maximus and quadratus lumbarum muscles against
mechanical membrane tension and electric stimulations conducted from 6 different
regions. As a result, reflex contraction responses in multifidus and longissimus muscles
were obtained by the electrical stimulation of lumbar afferents located in intervertebral
disc, zygapophyseal joint capsule and ligaments. This contraction response was highest
at the stimulation level. Similarly, the mechanical stimulation of viscoelastic structures
also caused contraction of muscles. In conclusion, the authors have stated that spinal
viscoelastic and ligamentous structures consisting of intervertebral discs, capsules and
ligaments had important roles in ensuring the kinesthetic perception in sensory cortex
and spinal muscle control [22].
Vertebral facet joints and proprioception
Vertebral facet joints are often named as apophysial or zygapophyseal joints. One facet
joint is formed by superior articular process of the lower vertebrae and inferior articular
process of the upper vertebrae. These are diarthrotic synovial type joints [7].
6
Electrophysiological studies conducted in recent years provide information on the
proprioceptive endings of facet and paraspinous connective tissues.
McLain et al., (1995) have conducted a study with the aim of investigating the type
and intensity of cervical, thoracic and lumbar spinal mechanoreceptor endings. In
the study, 36 facet joint capsules from the cervical, thoracic and lumbar vertebrae of
eight healthy cases were examined electrophysiologically. Findings have pointed to the
presence of neural elements associated with CNS within facet joint capsules. As a result,
four different receptors including Type I, Type II, Type III mechanoreceptive and Type
IV nociceptive receptors were observed located in the facet capsule in accordance with
Freeman and his colleagues’ classification. They have declared that these receptors had
a significant effect on protective muscle reflexes and joint pain, and also the density of
receptors in cervical region was higher than that in other segments. The reason of this
was suggested as the cervical segments being more mobile [12,14].
Spinal ligaments and proprioception
Spinal ligaments have a mechanical importance especially for the continuity of upright
posture and spinal stability. These structures are innervated by rich nerve endings. Spinal
ligaments give support to the active control of spinal balance by providing proprioceptive
feedback via neuromuscular reflex mechanism [25].
Ligaments of the spine [7]:
• Fibrous capsules of the facet joints
• Annulus fibrosus of the disc joints
• Anterior longitudinal ligament
• Posterior longitudinal ligament
• Interspinous ligament
• Supraspinous ligament
• Intertransverse ligaments
• Nuchal ligament
The effects of ligamentous structures on proprioception, motor control and stabilization
have been started to be discussed mostly with human and animal experiments in recent
years. In animal studies, the records obtained from ligaments and joint afferents have showed
that sensory outputs of ligaments have many different variations [26]. Most of the studies
about the innervation of the ligaments are focused in the knee joint. However, studies which
investigate the role of spinal ligaments over proprioceptive feedback mechanism are also
available [22,25].
In the studies about the innervations of the intervertebral disc, it is indicated that
mechanoreceptors located in posterior and anterior longitudinal ligaments in addition to
the ones on the external part of the annulus fibrosus are the proprioceptive structures
responsible for creating sense of movement and posture. Therefore, proprioceptive input
is negatively affected after intervertebral disc surgeries due to loss of tissue in both
annular fibers and longitudinal ligaments, which are among the most important parts of
proprioceptive structure [19].
Receptors within the ligaments have a low stimulation threshold against mechanical
stimulation, and become activated only when ligaments are stretched. While nerve endings
with high arousal threshold show slow adaptation against most stimuli, those with low
arousal threshold show both fast and slow adaptation. Ligaments with low excitation
threshold include the mechanosensitive nerve endings which have both static and dynamic
7
response capabilities. These nerve endings are responsible for providing information about
joint position and movement into the CNS. Afferents arising from joint mechanoreceptors
are projected to spinal motoneurons and interneurons before reaching to the supraspinal
structures.
Ligament afferents provide motor control and coordination through polysynaptic
interneuronal pathways and repetitive reflex activity of muscle spindle. However, functional
stability of joints (the stability during active movement) is formed as a result of limitation
caused by not only mechanical properties of ligaments but also the joint capsule, shape
of joint (geometry), friction between the surfaces of cartilage (gristle), body weight and
compression forces which muscle activity creates around the joint. In brief, functional joint
stabilization is provided by a mechanical and sensorial combination of the muscles and
ligaments [26].
Stubbs (1998) has conducted a study to evaluate the ligamentomuscular reflex
relationship located between paraspinal muscles and spinal ligaments. In this study
bipolar stimulation electrodes were placed to the supraspinous ligaments of six adult cats,
in pursuit of anesthesia and dissection. Reflex paraspinal muscle EMG responses that
occurred during supraspinous ligament stimulation were measured bilaterally on Lumbal
(L) 3, L4 and L5 level. Findings have showed that there was a protective ligamentomuscular
reflex resulting from lumbal supraspinous ligament mechanoreceptors and reaching out
paraspinal muscles [27].
According to the results of clinical research on patients with chronic low back and neck
pain, many different hypotheses regarding the injury mechanisms have been proposed. It is
thought that nociceptive sensors of the spine play a role on the basis of these hypotheses.
In addition, other spinal problems such as facet joint injuries, spinal column degenerations,
injury and clinical instabilities, inferior facet impingements in the laminas, Schmorl’s
nodules are also dwelled on.
Provided that a structural defect of the spine develops such reasons as degeneration or
injury, impaired structural stability will be tried to compensate with muscular stability.
The same situation is also valid for the injuries of ligaments (spinal ligaments, annular
fibers of intervertebral discs and facet joint capsule fibers). Reasons such as ligamentous
fatigue, static flexor posture and cumulative microtraumas lead to functional impairment
in the mechanoreceptors located in ligamentous structures. They cause to produce
false signals of neuromuscular control unit which regulates the amount of muscle
contractions by getting afferent information from these affected mechanoreceptors. As
a result of deteriorated muscle contractile function and coordination, a vicious cycle
occurs like overloading of the facet joints, abnormal loading of muscle and ligament
mechanoreceptors. This vicious cycle accelerates disc and facet degeneration by creating
problems in the healing process of spinal ligaments. The continuation of the negative
statements causes chronic low back pain depending on the inflammation of neural
tissues [17].
Muscles related to spinal regions and proprioception
Core stability of the body includes passive structures like thoracolumbar spine and
pelvis, and active structures like trunk muscles. Core stability of the trunk is stated
as perturbations’ coming from distal body parts either expectedly or unexpectedly,
and neuromuscular control which is formed against forces affected on the body,
internally or externally. Core stability can be also expressed as dynamic stability of
the trunk [28].
Muscle groups which can be also named as core muscles and play an active role in
sensory-motor control of the spine can be grouped as follows according to their properties
[7,18,29-32].
8
Local paravertebral
muscles
Global polysegmental
paravertebral muscles
•Intertransversarii
•Interspinous
•Multifidus
•Longissimus thoracis pars
lumborum
•Iliocostalis lumborum pars
lumborum
•Quadratus lumborum,
medial fibers
•Transversus abdominis
•Obliquus internus
abdominis (fibre insertion
into thoracolumbar fascia)
•Longissimus thoracis pars
thoracis
•Iliocostalis lumborum pars
thoracis
•Quadratus lumborum
lateral fibres
•Rectus abdominis
•Obliqus externus
abdominis
•Obliqus internus
abdominis
İntra abdominal basınç
üzerinde etkili olan
kaslar
•Abdominal muscles
•Pelvic floor
•Diaphragma
Local paravertebral muscles: These are the segmental muscles that are responsible for
the direct stabilization. Deep mono and oligoarticular intervertebral muscles (such as the
multifidus or interspinous muscles) provide internal stabilization or segmental stabilization.
They are automatically contracted by afferent stimulants coming from the intervertebral
joints and ligaments. Gamma spindle system plays an active role in this interaction
[7,16,18,31-34].
Global polysegmental paravertebral muscles: They are responsible for reducing and
balancing internal and external loads overlapping on the spine. Protection from these loads
and sustaining the stability are provided by muscles stretching at every level of intervertebral
joints and co-contractions of the antagonists. Co-activation is achieved by the inhibition of
interneurons in reciprocal pathways [7,16,18,31,33].
Affective muscles on intra-abdominal pressure: It can be mentioned about two
different hypotheses regarding the effectiveness of increased intra-abdominal pressure
on the regulation of the spinal position. The first hypothesis is the stability provided by
the viscoelastic property of the Thoracolumbal Fascia (TLF) [35], and the second can be
said as hoop-like hypothesis [29]. Transverse abdominus muscle extends to abdomen
horizontally and adheres to transverse process of the respective vertebrae through TLF. A
moment occurs inwardly with the contraction of this muscle in the front wall of abdomen.
This moment increases intra-abdominal pressure by compressing intra-abdominal cavity.
Increased intra-abdominal pressure stretches TLF. This stretching cause contraction of the
paravertebral muscles wrapped by the deep layer of TLF and provides lumbopelvic stability.
The diaphragm forms the roof and the pelvic floor forms the bottom of the core rigid
cylinder. These structures work like a valve. In the hoop like hypothesis, it is in question
that this valve system changes the intraabdominal pressure and as a result, the transversus
abdominis muscles, paravertebral muscles and TLF are stimulated [18,30,34].
Cholewicki et al., (2006) have conducted a study on 14 healthy volunteer cases with the aim
of evaluating proprioceptive changes in the lumbar spine kept inactive. Cases were assigned into
two groups randomly as one group with orthosis and the other without orthosis. Evaluations
were performed on the first (initial), seventh and twenty-first days. In this study, cases were
dressed Lumbo Sacral Orthosis (LSO-Aspen Medical Products, Inc, Long Beach, CA) at least
3 hours a day, during 3 weeks. Therapoint pressure measurement (Roho, Inc, Belleville, IL)
was used to standardize abdominal pressure of the corset. Device was placed in the space
between corset and abdomen (umbilicus lateral) by setting its pressure to 35 mmHg (4.7 kPa).
9
Cases were trained about remembering this pressure sense and using it whenever they wore
the corset. Proprioceptive assessment was made by the axial movements in L4-5 oriented
transverse planes in the sitting position, by using the same experimental setup by Lee et al.,
[1]. According to the initial neutral and changed positions of the cases, the angular deviations
the cases made during passive and active re-positioning (returning to neutral position) were
recorded. Consequently, the usage of LSO changed the values of proprioception. The reason of
this change was said to be time-dependent sensory-motor adaptation [36].
Thoracolumbar Fascia (TLF) and core muscle interaction
Both the static and functional/dynamic stabilization of the body during the activities like
walking, standing, sitting, reaching to somewhere etc. are needed. The force transmissions
are also needed biomechanically during displacements of body segments against gravity, from
active working extremity muscles to the trunk, pelvis and sacroiliac joint, in addition to receptor
mechanisms which have a role in neuromuscular control of the body. This transmission is
very important for the body to be positioned properly against the body’s gravitational changes.
In the biomechanical and electrophysiological studies, it is mentioned about the significance
of TLF during the transmission of muscle forces [18,35,37-39]. TLF surrounds the dorsal
muscles of the body. It starts from both sacrum and iliac bones and links up to linea nucha.
The superficial layer of TLF adheres to gluteus maximus, gluteus medius, external oblique,
latissimus dorsi and trapezius muscles. In addition, the deep layer of TLF adheres to gluteus
medius, erector spinae, internal oblique, serratus posterior inferior and sacrotuberous ligament.
Force transmission between the spine, pelvis and legs is provided by this connection between
TLF and these muscles. At the same time, the upper extremity and trunk movements (especially
rotation) transfer force to the lower lumbar vertebrae and sacroiliac joint by means of TLF.
Gluteus maximus and latissimus dorsi play role in the transmission of force between upper and
lower extremities. This transmission is provided by the superficial layer of TLF which connects
muscles to each other contralaterally by crossing the center line at L4-S2 level [40,41].
Vleeming et al., (1995) have talked about 3 muscle slings in connection with TLF [41]
(Table 2).
The anterior
oblique slings system
The posterior
oblique slings system
The lateral
slings system
The deep longitudinal
slings system
Hip adductors
Gluteus maximus
Hip adductors
Spinal erectors
Oblique abdominal muscles
Latissimus dorsi
Hip abductors
Biceps femoris
Abdominal fascia
Thoracolumbar fascia
Quadratus lumborum
Sacrotuberous ligament
Rectus abdominis
Sacroiliac joint
Sacroiliac joint
Sacroiliac joint
Table 2: Muscle slings in connection with TLF.
The roles of TLF in trunk neuromuscular control can be sorted in brief as follows;
• Viscoelastic resistance property [36].
• Transversus abdominis-Multifidus co-contractions [36,37].
• Force transmission between muscles [36,38].
• Help to posterior oblique sling system [36,38,39].
According to Jemmet (2004), muscles responsible for spinal stabilization are grouped
under three sets of muscles: the deep, middle and outer layer muscles (Table 3).
Deep layer muscles
Middle layer muscles
Outer layer muscles
The vertebrae, discs and ligaments and a
series of small muscles running from one
vertebrae to the next
Multifidus,
Quadratus lumborum,
Transversus abdominis
Psoas
Erector spinae,
External oblique abdominis,
Internal oblique abdominis,
Rectus abdominis
Table 3: Muscles responsible for spinal stabilization.
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In order to maintain the control of spinal muscles and stabilization of joints, the
nervous system is required to perceive even the tiniest changes in spinal joint position. This
subconscious position sense is the most important part of all body movements. According to
the recent studies, decrease in position sense lead to decrease in control of the middle layer
muscles and thus, in spinal stability [34].
Spinal muscles are postural muscles mostly consisting of type I fibers. It is known that
in type I muscle fibers, muscle spindle receptors are in high rate. Biomechanical changes
due to spinal problems can lead to the changes of proprioceptive perception by creating
faulty afferents from spinal mechanoreceptors and muscle spindles [42,43].
According to muscle-tendon vibration and microneurographic studies, muscle spindles
are indicated to be the most important structures responsible for proprioceptive sensory
perception. Muscle-tendon vibration is the most powerful stimulant of the muscle spindle
primary afferents [44].
Brumagne et al., (1999) have searched whether or not paraspinal muscle spindles
stimulated by means of a vibrator have an effect on lumbosacral position sense. Twenty-five
healthy subjects with ages ranging from 19 to 27 were included to the study, and randomly
assigned into two groups (16 people for experimental group, 9 people for control group).
The sacral tilt reposition angle of both groups was measured by using an electrogoniometer
through the sensor that is attached to the skin at the level of sacral 2 vertebras, in the
sitting position. Vibration was applied to the multifudus muscles of the subjects in the
experimental group, by a vibrator, for 5 seconds at 0.5 mm amplitude and frequency of 70
Hz. This application was not applied to the control group. In consequence of this study, the
importance of the stimulation of the paraspinal muscle spindles for perceiving the position
of lumbosacral spine and pelvis was shown [5].
In order to provide subconscious awareness of spinal motion, nerve endings of the spinal
discs and ligaments at each level send information to the nervous system related to the
position.
Neural control system regulates the muscle tension required for stabilizing and
maintaining disc and ligaments in the joint by using the information of this position sense.
Proprioception is the most important part of the neural control system containing the senses
of position and movement, and responsible for the perception of force, weight and timing of
muscle contractions [42,44].
Proprioception is associated with musculoskeletal injuries. Joint disabilities develop
as a result of the disability of different anatomical regions, tissue pathologies, pain and
musculoskeletal abnormal movements. The stability of the joint is provided by the alignment
of joint-bone components, integrity of noncontractile periarticular connective tissues and
power-producing muscles to facilitate or inhibit movement. While bones and ligaments have
an active role in static stability, muscles provide dynamic stability. An effective dynamic
stability requires more control than the force generated by muscle tension. Neural control
system plays a role in both selection of the muscles contracting and regulation of the
magnitude of the contraction force. The magnitude of this force should be at a level that
provides to set limits of joint movement and to process in a balanced way of agonistic and
antagonistic forces. This skill requires proprioception, also called as the sixth sense. The
decreased proprioception of trunk leads to delay in reaction-time and to the disorders of
postural control and stability [42,44].
Some of the problems which may cause proprioceptive disorders can be listed as follows
[42];
1. Age of the individual
2. Increased joint mobility or decreased joint stability
11
3. Muscle training, hypertrophy or atrophy
4. Muscle fatigue
5. Vibration
6. Regional neuromuscular trauma
a. Mechanical
i.
Tension/tensile (sprain, strain)
ii.
Compressive (edema, compartment syndrome)
b. Physiological
i.
Ischemia (compartment syndrome)
ii.
Denervation or reinnervation faults
iii.
Hematoma
7. Muscle fascicule length
8. Mechanoreceptor endowment density
9. Muscle contraction (pain and spasm)
10.Joint diseases
Spinal Stabilization, Postural Control and Proprioception
Postural control or stability is a skill to keep the gravity center of the body within the
support surface and stabilization limits. There are two important functions of the postural
control mechanisms. The first one is antigravity, and the other is communication function
with external environment.
Antigravitational property is to provide the stability of body segments against the forces
of gravity or ground reaction. For this process, muscle tonus, postural tonus and extensor
antigravity muscles are used [10,45].
According to available knowledge, in the regulation of body posture, three significant
body parts have proprioceptive importance. These are:
• Feet: It contains proprioceptors located in the feet sole and intrinsic leg muscles which
produce information about the position of leg and ankle joint.
• Head and neck: It contains labyrinth and neck proprioceptors which form the basis of
visual organs, neck and labyrinth reflexes.
• Trunk: It contains graviceptors which form the basis of lumbar postural reflex and
exist around kidney [10,45].
Feet
Plantar foot sole receptors are important in the perception of body loads or weight.
Another load receptor is the golgi tendon organ which monitor the muscle work during
counteraction against the gravity force.
In order to provide postural control, afferent inputs generated by the multisensors
(visual, labyrinth, proprioceptive, cutaneous and graviceptive, etc.) which perceive body
schema (geometry, weight, verticality, etc.) are processed by the postural network, and are
used for neuromuscular control.
During movement, consistently changing positions of head, trunk, and extremities are
12
processed easily by these systems and the adaptation of body to these changing positions
is provided [45,46].
Head and Neck
The reference point for interaction function with the external environment is the position
of the head. Head has an important role in determining the trajectory of activities such as
reaching and catching, and in spatial orientation of the segments like trunk and arm in
regulating body movement according to the external environment [46].
Neck proprioception produces information about the position changes of shoulder girdle,
and the trunk proprioception produces information about the position changes of extremity
girdle and trunk. The structures of trunk responsible for producing information about the
plane changes in the anterior-posterior and/or medio-lateral direction are trunk muscles.
At the same time, these muscles enable lower extremities to correctly perform their duties of
supporting the body in vertical position and moving it forward. Participation and control of
trunk muscles required for the dynamic balance of the body is higher than for the statical
balance [47].
The neck stability is affected from ground reaction forces and constant gravity forces
which are formed by asymmetric movements of the lower extremity in stance and swing
phases of walking. According to Newton’s laws, linear or angular changes occurring in
a structure cause reverse movements in the attached or adjacent segments. In actions
involving the movement of the body such as walking, the torque force moments occurring
with the influence of gravitational forces play an important role in the deterioration of the
head stability. The passive mechanisms (stability provided by the vertebrae, the viscosity
and stiffness provided by the ligamentous and capsular structures), reflex mechanisms
(vestibulocollic, cervicocollic) and voluntary responses (neck muscle contractions) play
important roles in counteracting this torque forces. CNS controls this reflex and muscular
interaction [47,48].
Trunk
Spinal stability can be provided by the management of the neuromuscular system.
Neuromuscular control can be expressed as the control and coordination between the
Central Nervous System (CNS) and sensory-motor systems of the musculoskeletal system
(Peripheral Nervous System - PNS). By means of this control, the functional or dynamic
stability of the joint is achieved through involuntary contractions of the muscles as a
response to the loads generated by the internal or external forces during movements
[10,45,46].
Spinal proprioception can vary according to the plane it stands. That means the
spinal proprioception of a person can vary in the positions of standing (axial axis) or lying
(transverse plane). Spinal pathologies can also change proprioceptive perception thresholds.
Lee et al., (2010) have investigated the effects of spinal pathology and spinal position
on trunk proprioception on 24 volunteers with low back pain and 24 healthy controls.
Proprioception measurements were performed in three different positions as sitting (backsupported and feet on the ground), supine and side-lying. For the measurement in sitting
position, a chair with upper part fixed and seating part movable by a motor located in its
bottom was used. For side-lying and supine position measurements, a bed with upper part
(supporting the head and upper trunk) fixed and lower part (supporting the lower body)
movable by a motor was used. Neutral initial positions for three positions were determined,
and during the tests, the lower trunk positions of the subjects were changed, and brought
to different angles from the neutral position. In the meantime, upper trunk and head were
fixed to the chair and bed with band systems in order to eliminate the vestibular perception.
The visual perception was eliminated by closing the eyes, and auditory perception of motor
13
sound was eliminated by listening to music. Lumbal axial rotation (sitting), lumbal flexion/
extension (side-lying) and lateral flexion (supine) movements of the subjects were evaluated.
The initial neutral position angles of the cases were changed, and their thresholds of passive
movement perception and the amount of angular errors during passive and active repositioning (returning to neutral position) were recorded. Consequently, passive movement
perception threshold was found to be higher in subjects with low back pain compared to
healthy controls, in all positions. In addition, the passive movement perception threshold
for all subjects in the transverse plane was higher than that of in the axial axis. Passive and
active re-positioning (return to neutral position) angular errors were similar between groups.
Active repositioning errors were found less compared to passive repositioning errors. In
consideration of these findings, spinal proprioception can be said better in vertical position
and in the conditions where positions were done actively [1].
There is a close relationship between spinal stabilization and function. Trunk provides
both dynamic and static stabilization for different parts of body. According to many studies,
it is reported that the risks of injury in other segments of the body can increase in the
inadequacy of spinal neuromuscular control [28,49-51].
Barrac et al., (1984) have investigated the effect of idiopathic scoliosis on proprioception.
In this study, 20 healthy subjects and 17 idiopathic scoliosis patients were assessed. The
angular change threshold of knee joint was recorded as a measure of proprioception. As a
result, proprioception results of scoliosis patients were found worse than the control group
values [52].
Zazulak et al., (2007) have studied the relationship between injuries of the knee joint and
delayed spinal muscle reflex responses in their study on 277 elite athletes. For this purpose,
the athletes have been watched in terms of the number and region of injuries for 3 years.
In order to evaluate neuromuscular control of trunk, the responses of subjects’ delayed
spinal muscle reflex were measured by EMG against the sudden moments formed in the
direction of flexion-extension and lateral flexion. As a result, they have found that there was
a relationship between delayed trunk muscle responses, decreased proprioceptive input and
rupture of knee ligaments, especially in elite female athletes. Accordingly, they have stated
that decreased trunk proprioception could be used for predicting knee injuries [28].
Cholewic et al., (2005) have investigated in their study on 292 athletes whether there
was a relation between lower back disabilities and delayed spinal muscle responses. For
this purpose, athletes have been followed for 2-3 years in terms of low back injury. In order
to evaluate delayed trunk muscle responses, EMG responses from 12 large trunk muscle
groups were used against sudden flexion, extension and lateral flexion moments which were
formed through the electromagnet pulley system. EMG measurements have been made
through rectus abdominis (3 cm lateral to the umbilicus), external oblique (approximately
15 cm lateral to the umbilicus), internal oblique (approximately midway between the anterior
superior iliac spine and the symphysis pubis, above the inguinal ligament), latissimus dorsi
(lateral to T9 over the muscle belly), thoracic erector spinae (3 cm lateral to T9 spinous
process), and lumbar erector spinae (3 cm lateral to L4 spinous process) muscles. According
to the data obtained from the study, the delayed spinal muscle responses have been
concluded to be a predisposing factor to low back injuries and pain [51].
Hübscher et al., (2010) have searched the literature on the effectiveness of neuromuscular
training on the prevention from sports injuries. According to the results of this research,
evidences were obtained regarding that exercise programs that include training of balance,
proprioception and spinal stabilization decreased the risks of lower extremity injuries [50].
It is seen that the number of animal and human studies searching proprioceptive
properties of spinal structures is less than the studies done for the extremities. Clinical
trials are generally focused on the measurements of reflex responses against stimulation,
14
the delayed spinal reflex responses against vibration and spinal stability [3,5,24,2628,44,47,51,53]. Even if the studies are limited in number, they indicate that the conservation
and development of spinal proprioception are effective on postural control, balance, static
stability, functional stability and the prevention from injury in other body parts [50-53].
There is a need for further studies on this subject.
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