OSSEOPERCEPTION:
SENSORY FUNCTION AND PROPRIOCEPTION
I. KLINEBERG*
G. MURRAY
Neuromuscular and Orofacial Pain Research Unit
Faculty of Dentistry, University of Sydney
Westmead Hospital Dental Clinical School
Westmead NSW 2145, Australia
* Corresponding author
Adv Dent Res 13:120-129, June, 1999
Abstract— Tooth loss and its replacement have significant
functional and psychosocial consequences. The removal of
intra-dental and periodontal mechanoreception accompanying
tooth loss changes the fine proprioceptive control of jaw
function and influences the precision of magnitude, direction,
and rate of occlusal load application. With the loss of all teeth,
complete denture restoration is a compromise replacement
which only partially restores function. Implant-supported
prostheses restore jaw function more appropriately, with
improved psychophysiological discriminatory ability and oral
stereognosis. Osseoperception is defined as depending on
central influences from corollary discharge from cortico-motor
commands to jaw muscles, and contributions from peripheral
mechanoreceptors in orofacial and temporomandibular tissues.
The processing of central influences is considered with the
recognition of the plasticity of neuromotor mechanisms that
occurs to accommodate the loss of dental and periodontal
inputs.
Key words: Edentulous, implant, osseointegration,
somatosensory, plasticity.
Presented at the 15th International Conference on Oral
Biology (1C0B), ((Oral Biology and Dental Implants", held in
Baveno, Italy, June 28-July 1, 1998, sponsored by the
International Association for Dental Research and supported
by Unilever Dental Research
120
T
he presence or absence of teeth and the status of their
replacement are highly significant. Complete
edentulism, as the end-point of tooth loss, is of itself
a major consequence, with progressive resorption
and remodeling of alveolar bone over time and the collapse of
unsupported lips with associated change in facial form. The
quality of the replacement prosthesis (a complete denture) may
or may not adequately restore function, esthetics, or social
well-being. Regardless of the technical excellence of such
prostheses, they are inherently unstable during normal
functional jaw movements. Fig. 1 shows, for example, the
extent of movement of a well-constructed complete upper
denture during chewing. Further, the management of complete
dentures becomes a problem from time to time in most
edentulous individuals. With age, these problems are
magnified (Brill et al, 1974) as soft tissues become friable and
resorbed bone less adaptable. As a consequence, mastication
becomes difficult, sometimes painful, and diet and nutrition
suffer. In the elderly, this is a major factor in their survival
capabilities, emotional stability, and general health, is
increasing with the "greying of the community", and is often
overlooked as a significant social problem.
Edentulous individuals also lack an important source of
tactile sensory input to the central nervous system (CNS), the
periodontal mechanoreceptors. In dentate individuals,
periodontal mechanoreceptors (PDMs) are thought to play a
key role in sensory discriminative capabilities and in the
control of jaw function, and as a result have been of special
interest in neurophysiological studies in animals {e.g., Hannam
and Matthews, 1969; Linden and Scott, 1989a,b; Bonte et al,
1993; Dong et al, 1993; Tabata et al, 1995; for review, see
Linden, 1990a,b; Maeda and Byers, 1996; Byers and Maeda,
1997) and man (Trulsson et al, 1992; Trulsson and Johansson,
1996; Turker et al, 1997), as well as psychophysical studies
assessing oral tactile function (for review, see Jacobs and van
Steenberghe, 1994).
Following tooth extraction, although periodontal tissues
break down and are absorbed, some PDMs remain within the
bone. Further, responses can be recorded in the trigeminal
mesencephalic nucleus following electrical, but not
mechanical, stimulation of the bone (Linden and Scott, 1989b).
The lack of response of PDM remnants to mechanical
stimulation, however, suggests that they are unlikely to be of
any further functional significance. This issue was also
comprehensively investigated in relation to the possibility of
reinnervation in association with titanium implants
(NobelBiocare, Gothenburg, Sweden) (Bonte et al, 1993). No
evoked responses were identified that could be attributed to
reinnervation in association with controlled forces directed to
implants placed in former tooth extraction sites.
The opportunities that are now available for implant-
supported anchorage of fixed bridgework for full-arch or
VOLB OSSEOPERCEPTION 121
segmental restorations and, as a Procedure: Right Side Chew Apricot
result, the provision of function
and esthetics that were not Maxillary Denture Movement
previously considered possible are (Jaws 3D)
in stark contrast to the "complete- x= + right
y= + anterior
denture era". Patients with implant- z= + superior
supported prostheses report
Displacement (mm)
improved tactile discriminative
capabilities and improved motor
function compared with when they at upper
wore complete dentures, although mid incisor — Y
their sensory and motor capabilities point — X
do not appear to match those of
dentate individuals.
The aims of this paper are (a) to
review the tactile sensory discrim- at post dam
inative capabilities of patients with
implant-supported prostheses, and
(b) to outline some possible neural
bases for these sensory capabilities.
at lower — X
7
SENSORY mid incisor
Y
point
DISCRIMINATION
Time (sees)
IN IMPLANT-SUPPORTED
PROSTHESES
Mandibular Movement
Periodontal mechanoreception (Sirognathograph)
provides feedback of magnitude, x= + superior
direction, and rate of occlusal load y= + right
application for sensory perception z= + anterior
and motor function. In addition,
intradental mechanoreception pro- Fig. 1—Maxillary complete denture movement. Recordings are displayed of maxillary
vides subtle modulation of occlusal denture movement in one subject with a complete maxillary denture opposed by a lower
loading for further refinement of partial denture with bilateral free-end saddles. A Sirognathograph (Siemans AG, Bensheim,
the neuromotor control of jaw Germany) was used to monitor mandibular movement (magnet attached to the lower incisor
function. With tooth loss, these fine teeth; data plotted in the lowest graph), while a JAWS3D (Metropoly AG, Zurich,
proprioceptive control mechanisms Switzerland) optoelectronic tracking system monitored the position of the maxillary denture.
are absent. Several studies of oral Points selected on the denture for monitoring displacement were the mid-incisor point and
tactile function have attempted to mid-post dam point. Subjects chewed a fibrous food (dried apricot), and two chewing cycles
quantify the loss of periodontal are displayed (see lower mid-incisor point movement, x-axis). The tracings confirm
mechanoreception in complete- significant maxillary denture movement at the mid-incisor and mid-post dam points.
denture and implant-restored Movement was maximal at the mid-incisor point (1.1 ±1.9 mm) and minimal at the mid-post
situations. dam point (0.3 ±0.2 mm). Maximal jaw displacement in chewing is shown to be of the order
A comparison of occlusal force of 4.0 mm vertically (x-axis) and 2.0 mm antero-posteriorly (z-axis) and mediolaterally (y-
levels between subjects with axis). Analysis of these data indicates that even if the maxillary denture is comfortable and
complete dentures and those with fits well, its movement in function is considerable. Movement of a lower complete denture
implant-supported prostheses found would be significantly greater (Kramer et al., unpublished observations).
a significant increase in maximum
bite force generated in implant-
restored subjects (Haraldson et al., 1979; Lindquist and mechanoreception must have a direct bearing on tactile
Carlsson, 1986; Carr et al., 1987). Additionally, the decrease in discrimination. Passive discrimination is dependent on
bite force was directly proportional to the duration of periodontal mechanoreception and is assessed by the
edentulism. application of controlled forces to a tooth, while active
Oral tactile function has been studied extensively discrimination is based on objects placed between teeth, and
(Muhlbrandt et al., 1989; Jacobs and van Steenberghe, 1991, involves a number of mechanoreceptor inputs located in teeth,
1993; Jacobs et al., 1992; Hammerle et aL, 1995) for periodontium, jaw muscles, and temporomandibular joint
comparison of implant-supported prostheses with natural teeth (TMJ) capsules and ligaments. Both active and passive
and complete dentures. The presence or absence of periodontal discriminative abilities decrease with age. Karayiannis et al.
122 KUNEBERG & MURRAY
(1991) found passive discrimination of osseointegrated
implants to be lOx higher than that of natural teeth (3.4 N and
0.3 N, respectively), while Jacobs and van Steenberghe (1993)
found the implant threshold to be 50x higher than that of
natural teeth.
In the passive psychophysical discrimination test of
magnitude estimation (where forces are applied to teeth and
compared with a previously applied standard force), implant-
restored responses are compared and contrasted with those of
natural teeth (Muhlbradt et al, 1989). It was found that there
were no significant differences in sensitivity as described by
the power function (the relationship between the applied force
and the estimated force level) between dentate and implant-
restored subjects. In contrast, the active discrimination
threshold for micro-thickness detection has been shown to be
lowest for natural teeth and is clearly dependent on the
precision provided by periodontal mechanoreception (ca. 8
|xm, Siirila and Laine, 1963; ca. 20 fxm, Jacobs and van
Steenberghe, 1991), higher for osseointegrated implant bridges
(ca. 50 |Jim, Lundqvist and Haraldson, 1984), and significantly
higher for complete-denture wearers (ca. 100 jxm). However,
with macro-thickness detection (100 |xm), there was no
statistically significant difference between implant
overdentures and complete dentures (Jacobs and van
Steenberghe, 1991).
Interpretation of psychophysical responses in the
determination of active interocclusal thresholds is confounded
by a number of factors, including subject variables (perceptive
discriminative ability, age, health, occlusal features),
experimental design, and the physical properties of the test
materials (aluminum, tin, lead, acrylic resin, polyester). An
assessment of interocclusal foil hardness and the influence of
temperature (Jacobs et al, 1992) addressed factors that had not
previously been considered. They showed that the material
used and its temperature (from 20° to 35°C) significantly
influenced the response. The active detection threshold for all
metal foils was found to be 16.3 ± 6.0 [im; the passive
detection threshold was 3.0 ± 2.2 g. Foil at room temperature
may serve as a cold stimulus with temperature transfer from
tooth to foil with possible activation of pulpal thermosensitive
units. The conductivity of the material used in psychophysical
tests varies significantly, and the influence of foil temperature
and its conductivity needs to be considered in the assessment
process (Jacobs et ah, 1992).
Oral stereognosis is the identification of objects of various
shapes which are placed between the teeth in the absence of
other sensory input (such as visual cues). Such tests have been
used for assessing complete-denture satisfaction (Berry and
Mahood, 1966). Oral stereognostic acuity decreases with
increasing age, but the duration of edentulism does not appear
to influence this ability (Mantecchini et al., 1998). It is likely
that with tooth loss, muscle spindle afferents provide the
dominant control (McCloskey, 1978), supported by afferent
inputs from temporomandibular joint (TMJ) capsules and
mucosal mechanoreceptors.
A comparison of teeth and implants confirmed the superior
stereognostic ability of dentate subjects and its marked
reduction, to a similar degree, in both complete dentures and
ADV DENT RES JUNE 1999
implant overdenture subjects (Jacobs et al., 1997). Periodontal
and intradental mechanoreception allows for a high degree of
precision in oral stereognosis. The reduction in stereognostic
ability following tooth loss is not surprising, but the
adaptability of the neuromuscular system in maintaining this
subjective interpretive skill is remarkable.
CONCEPT OF OSSEOPERCEPTION
Perceptions of static jaw position and velocity of jaw
movement (whether imposed or voluntarily generated) and
forces generated during contractions of the jaw muscles
constitute oral kinesthetic and proprioceptive sensations
(definition modified from McCloskey, 1978). While there has
been extensive study of the neural basis of limb kinesthetic
sensibility (for review, see McCloskey, 1978; Clark and
Horch, 1986), we have much less understanding of the neural
mechanisms of oral kinesthesia in dentate individuals and even
less understanding of the neural basis of kinesthetic perception
in patients with implant-supported prostheses who lack
periodontal mechanoreception.
The CNS has two mechanisms for obtaining information
about the positions and movements of limbs and forces of limb
muscle contraction, i.e., limb kinesthesia (McCloskey, 1978;
Clark and Horch, 1986). These mechanisms are also likely to
operate for oral kinesthetic perception.
(a) The first is by monitoring a corollary discharge (or
efference copy or collateral discharge) of the
descending central command to muscles. This
mechanism is thought to provide the sensation of
muscular force or effort which accompanies centrally
generated voluntary motor commands (McCloskey,
1978, 1981; Bennett, 1997). Corollary discharge,
possibly together with an input from Golgi tendon
organs (GTOs) associated with the jaw-closing muscles,
is therefore presumably important in the sensation of
effort in voluntary biting. In studies of limb kinesthetic
sensation, subjects appear to use corollary discharge in
judging muscular tension or the weights of lifted objects
(McCloskey, 1978). Corollary discharge, however, does
not provide a sensation of movement or altered position.
(b) The second mechanism is derived from
mechanoreceptors activated during limb and jaw
movements and at different limb and jaw positions. In
the context of implant-supported prostheses, the term
osseoperception was proposed (P-I Branemark, personal
communication) to recognize oral kinesthetic perceptual
abilities, in the absence of a functional periodontal
mechanoreceptive input. This input is derived from
temporomandibular joint (TMJ), muscle, cutaneous,
mucosal, and/or periosteal mechanoreceptors, and
provides mechanosensory information for oral
kinesthetic sensibility in relation to jaw function and
artificial tooth contacts. The relative contributions of
these different mechanoreceptors to osseoperception in
patients with implant-supported prostheses are unclear.
Although periodontal mechanoreceptors may remain
VOL. 13
functional in bone in the vicinity of the implant fixture,
it appears unlikely that these mechanoreceptors make
any contribution to osseoperception.
MECHANORECEPTORS
CONTRIBUTING TO OSSEOPERCEPTION
(a) Joint mechanoreceptors
Low-threshold mechanoreceptors are present in the TMJs of
experimental animals and humans (Thilander, 1961;
Klineberg, 1971; Dubner et al., 1978) and in other joints of the
body (for review, see McCloskey, 1978). While it is generally
considered that joint receptors play a limited role in signaling
movements and positions of limb joints (McCloskey, 1978;
Clark and Horch, 1986; Proske et aL, 1988), and appear to be
more concerned with protective reflexes (limb-joint receptors
appear to be mainly active at the extremes of joint movement),
it appears that TMJ receptors may play a more significant role
(Klineberg, 1980; Lund and Matthews, 1981). A population of
receptors has been described in the TMJs of rabbits; these have
been classified as limited-range receptors (Lund and
Matthews, 1981) and, unlike those of the knee joint (for
reviews, see McCloskey, 1978; Clark and Horch, 1986), most
were readily excitable during the mid-ranges of TMJ
movement rather than being maximally excited at extreme
joint positions. These receptors therefore could potentially
provide detailed information as to jaw position and movement.
(b) Muscle mechanoreceptors
The two principal mechanoreceptors associated with muscle,
GTOs and muscle spindles, are slowly adapting receptors.
• Golgi tendon organs are found at the musculo-tendinous
junction in series with a small number of extrafusal
muscle fibers, and the pull of the muscle fibers with
muscle contraction activates GTOs. Golgi tendon
organs have been reported in jaw muscles (for review,
see Dubner et aU 1978; Capra and Dessem, 1992), and
their physiological properties (Lund et ai, 1978) appear
to be similar to those described for limb muscles
(Proske, 1981; Clark and Horch, 1986; Jami, 1992). In
contrast to the role of the GTOs as high-threshold and
monitoring overload, it is now recognized that they
have very low thresholds to muscle contraction (Proske,
1981; Clark and Horch, 1986; Jami, 1992) and provide
detailed information concerning the magnitude of
muscle contraction. They clearly play an important role
in regulating muscle contraction and are the most
appropriate mechanoreceptors for signaling
intramuscular tension (McCloskey, 1978; Proske, 1981;
Clark and Horch, 1986). These receptors, together with
corollary discharge, are likely to make important
contributions to the sense of intramuscular tension
generated during voluntary contractions such as biting.
• Muscle spindles are the most complex somatosensory
receptor in the body with sophisticated physiological
properties (for review, see Barker and Banks, 1994),
and they provide detailed information on muscle length
and rate of length change. Spindles lie in parallel with
OSSEOPERCEPTION 123
extrafusal muscle fibers, have independent sensory
innervation, and contain specialized intrafusal fibers
with direct motor innervation from fusimoto- (7- moto-)
neurones. With 7-motoneurone discharge, the
contraction of intrafusal fibers contributes to an
increased spindle afferent discharge. During voluntary
muscle contraction, both a and 7 motoneurones are
activated simultaneously (a-7 co-activation), which
ensures that muscle spindles maintain their high
sensitivity without saturation over a wide range of
muscle lengths.
Intramuscular receptors, probably the primary and
secondary spindle afferents, are now recognized as important
monitors of limb position and movement (McCloskey, 1978;
Clark and Horch, 1986). It is likely that intramuscular
receptors in jaw muscles perform a similar function in the
assessment of jaw position and movement. However, given the
superior tactile discriminative abilities of dentate subjects in
comparison with those with implant-supported or removable
prostheses, periodontal mechanoreceptors provide a more
sensitive indicator of jaw position and movement.
The presence of a 7-motoneurone innervation of muscle
spindles complicates the interpretation by the CNS of afferent
information from them. There needs to be a mechanism
whereby the CNS can distinguish between spindle afferent
discharge that has arisen from 7-motoneurone activation, and
afferent discharge from an actual change in muscle length. It
appears that the CNS uses its own motor signals (via corollary
discharge) to determine the contribution made to spindle
afferent signals from 7-motoneurone drive (McCloskey, 1978;
Clark and Horch, 1986; Matthews, 1988). The resultant signal
is used by the CNS as an unambiguous signal of muscle length
and muscle length change and therefore, in the absence of
periodontal afferent input, can provide detailed information on
jaw position and movement.
(c) Cutaneous mechanoreceptors
There has been much discussion of the possible roles of
cutaneous receptors in kinesthetic sensations. There is,
however, little information on the magnitude of skin
deformation caused by associated joint movements, and it is
not clear how cutaneous receptors respond to such
deformations (Edin, 1992), or what contributions to kinesthesia
are made by cutaneous receptors. Whether the information
provides kinesthetic perception or a general facilitatory
influence on afferent projections from other mechanoreceptors
from muscle and joint needs to be determined.
Recent evidence confirms the exquisite dynamic and static
sensitivity to skin stretch of slowly adapting type I and type II
mechanoreceptors from the hairy skin of the hand in humans
(Edin, 1992; see also Vickery et aL, 1994; Gynther et al.,
1995). These receptors were shown to display a positional
sensitivity that was comparable with that reported for muscle
spindle afferents (Edin, 1992). The findings support the
suggestion that cutaneous mechanoreceptors in human hairy
skin have the potential to provide detailed information on
underlying joint movements, which may be important in
kinesthetic perception.
124 KUNEBERG & MURRAY
Fig. 2—Somatotopic organization
within sensorimotor cerebral
cortex. (A) A diagrammatic
representation of the somatotopic
organization within the
somatosensory cortex of
mechanoreceptive afferent input
from the body surface. (B) The
somatotopic organization within
the primary motor cortex of outputs
projecting to muscle. The extensive
cortical sensory and motor
representation of the orofacial
region (tongue, teeth, jaws, lips,
and face) is thought to be essential
for orofacial tactile and kinesthetic
acuity and for motor function (from
Penfield and Rasmus sen, 1950).
Cutaneous receptors in the hairy skin overlying the TMJ
may also respond to skin deformation occurring during
condylar movements. While there is no direct evidence for this,
facial skin and mucosal mechanoreceptor activities recorded
from the infra-orbital nerve exhibit vigorous discharges during
facial movements (Johansson et al. 1988a,b), and
somatosensory thalamic neurones with lip and tongue
mechanoreceptive fields have been shown to be consistently
activated during speech (McClean et al. 1990). This
somatosensory input may provide important proprioceptive
information for the control of facial muscles which are known
to lack definitive muscle spindle innervation (Johansson et al.,
1988a,b; Mclean et al, 1990). It is also likely that orofacial
cutaneous mechanoreceptors exhibit response properties similar
to those described in detail for the limbs for which five
cutaneous mechanoreceptor classes have been identified (for
reviews, see Darian-Smith, 1966, 1984). These properties
include low thresholds to applied mechanical stimuli and
graded increases in firing rate with the magnitude of the applied
mechanical stimulus (for reviews, see Darian-Smith, 1966,
1984). Such response properties may therefore provide
information to the CNS concerning jaw position and
movement.
(d) Mucosal mechanoreceptors
Where natural teeth are present, periodontal mechanoreceptors
are important for refined interdental discriminative function
(Linden, 1990). With implant-supported prostheses opposing
complete dentures, a contribution to oral kinesthetic perception
could come from the activation of mucosal receptors beneath
the complete denture and possibly periosteal and/or mucosal
mechanoreceptors in the vicinity of the implant fixture (Jacobs
and van Steenberghe, 1991). As with facial cutaneous
receptors, intra-oral mucosal receptors have not been
characterized electrophysiologically; however, they too are
likely to show low thresholds and graded responses to
mechanical stimuli that could contribute to assessments of
position and velocity of jaw movement at tooth contact, as well
ADV DENT RES JUNE 1999
as force of muscular contraction by their activation beneath
complete dentures during occlusal loading.
(e) Periosteal mechanoreceptors
There are few physiological data on the potential role of
periosteal mechanoreceptors in kinesthetic perception (for
reviews, see Sakada, 1983; Capra and Dessem, 1992).
CENTRAL PROCESSING OF SOMATOSENSORY
INFORMATION FOR OSSEOPERCEPTION
(a) Central neural representation
There have been considerable advances in our understanding of
how the brain processes somatosensory information from
superficial and deep receptors in the forelimb and hindlimb for
tactile perception, kinesthesia, and motor control (McCloskey,
1978, 1981; Darian-Smith, 1984; Mountcastle, 1984; Clark and
Horch, 1986; Chapman, 1994; Kaas, 1996; Rowe etal, 1996).
However, there is comparatively little information as to how
orofacial somatosensory information is used by the brain not
only for kinesthetic perception, but also for tactile perception,
oral stereognosis, and motor control (Kawamura, 1983;
Morimoto, 1990; Hannam and Sessle, 1994). Nonetheless, there
is good evidence for an extensive representation within the
CNS of a wide range of somatosensory orofacial inputs,
including those from cutaneous and mucosal mechanoreceptors,
muscle spindles, and GTOs associated with jaw muscles, as
well as TMJ and periodontal mechanoreceptors. These
representations have been demonstrated at various levels of the
orofacial somatosensory afferent pathway, including the
trigeminal sensory nucleus, the ventroposteromedial (VPM)
nucleus of the thalamus, and the primary somatosensory cortex
(SI) in a number of animal species (e.g., Darian-Smith, 1966,
1984; Dubner et al, 1978; Huang et al, 1989; Capra and
Dessem, 1992; Manger et al, 1995, 1996) and in the human
(McClean et al, 1990). Further, there is evidence that this
information is used for reflexes (Dubner et al, 1978; Lund,
1990), for the modulation of central pattern generators for
V0L.1S OSSEOPERCEPTION 125

mastication and swallowing (Jean, 1984; Rossignol et aim
1988), for the refinement and control of voluntary orofacial
movements (Murray and Sessle, 1992a,b), and for the
perceptual functions of oral kinesthesia, oral stereognosis, and
tactile perception (Kawamura, 1983; Capra and Dessem, 1992;
Jacobs and van Steenberghe, 1994). Although it is unclear how
the CNS processes sensory information in these various
functions, it is likely that afferent information from several
receptor classes is integrated and processed.
(b) Mechanoreceptor projection to somatosensory cortex
For mechanoreceptive information to reach conscious
perception, it must project to the cerebral cortex. In particular,
access of somatosensory information to the primary
somatosensory cortex (SI) appears crucial for perception.
There is evidence of the importance of the primary
somatosensory cortex (SI) in tactile acuity, detection, and
discrimination of sensory information from the limbs (Penfield
and Rasmussen, 1950; Mountcastle, 1984; Kaas, 1996).
Although there is much less information as to the role of the
face SI in primate orofacial somatosensation, it appears to be
equally important for orofacial somatosensory processing
related to perceptual processes (Penfield and Rasmussen,
1950; Dubner et al, 1978; Mountcastle, 1984).
There is now evidence that joint, muscle, and cutaneous
afferents from the limbs project to
somatosensory cortical areas Boatral
(McCloskey, 1978; Mountcastle, 7 4
1984; Wiesendanger and Miles,
1982; Jami, 1992) and evidence for
Med.
the projection of cutaneous, 3-
mucosal, and deep receptors to the
face sensorimotor cortex (Woolsey
4-
et al., 1952; Dreyer et al., 1975;
Huang et al., 1989; Murray and
Sessle, 1992a; Manger et al, 1995, S--
6 -
Fig. 3—Representation of orofacial
1996; see Figs. 2 and 3). An extensive cortical representation
of cutaneous, mucosal, and deep somatosensory afferents
could contribute, in the absence of periodontal afferents, to
conscious perceptual experiences associated with kinesthetic
sensibility.
(c) Security of transmission of mechanoreceptive
information to the somatosensory cortex
Much of this mechanoreceptive information is capable of being
transmitted along somatosensory afferent pathways with high
synaptic security (it has been demonstrated that a single action
potential recorded in an afferent nerve fiber from a single
Pacinian corpuscle is capable of generating an evoked potential
in limb SI). Recent data have convincingly illustrated the
potency of synaptic transmission across the first synaptic relay
in the dorsal column nuclei for somatosensory information from
Pacinian corpuscle afferents (Ferrington et al, 1987), slowly
adapting receptors (Vickery et al, 1994; Gynther et ai, 1995),
muscle spindles (Mackie and Rowe, unpublished observations),
and wrist joint mechanoreceptors (Coleman and Rowe,
unpublished observations). The potency of transmission of
information is underscored by the observation that a single
action potential along any one of these afferent fibers can evoke
one or more action potentials in the central recorded neurone.
This high security of transmission has now been demonstrated
H3 LT
3 0 4 mil
area 3
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areal area 2
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somatosensory inputs within face

somatosensory cortex. Low- 7--
threshold mechanoreceptive AAAAA A
afferents inputs to the face SI region 8 • oooo fooo g oo
were mapped with microelectrodes oooo /oooooo oo AA
in the left post-central cortex of a
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O O O A
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top of the caudal bank of the central 10- •••••••••*
sulcus; the dashed line indicates the #
bottom of the central sulcus. Cy to-
11 a
LaCl AAAAA
architectonic boundaries among
areas 3, I, and 2 are indicated by
black continuous lines. Symbols INPUT
indicate the recording sites of A upper lip A tongue
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the regions indicated at the bottom region
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126 KLINEBERG & MURRAY
at higher levels of the somatosensory afferent pathway—for
example, at the ventroposterolateral (VPL) thalamus (spinal
equivalent of VPM thalamus; Rowe et aL, unpublished
observations) and somatosensory cortex (Rowe and Zhang,
unpublished observations).
Although there are no studies concerning the security with
which somatosensory information from the orofacial region is
conveyed to the cerebral cortex, the same security of
transmission is also likely to operate for orofacial
somatosensory information. The data indicate that in the
absence of periodontal input, there is the potential for the rich
somatosensory information within the orofacial area to gain
access, with high synaptic security and potency, to these
cortical areas for kinesthetic and tactile perception and motor
control.
(d) Gating of somatosensory input
Somatosensory cortical regions appear to be able to control the
gain of transmission of somatosensory information to the
somatosensory cortex (Ghosh et aL, 1994; Lin and Sessle,
1994) and thereby play a role in selective attention to specific
somatosensory stimuli (Ghosh et aL, 1994; see also Chapman,
1994).
Patients with modified somatosensory input following tooth
extraction and the subsequent restoration with implant-
supported prostheses, instead of complete dentures, may
accommodate to the new intra-oral environment by selectively
attending to specific orofacial afferent information in the
functional accommodation of the new prosthetic appliances.
The fitting of implant-supported prostheses will evoke a
change in somatosensory input to the brain that will be
markedly different from that occurring with complete
dentures. Somatosensory cortical areas may play a role in
focusing attention on these specific sensory inputs derived
from orofacial mechanoreceptors and provide a framework for
the individual to accommodate to this altered intra-oral
environment.
(e) CNS plasticity to accommodate
to loss of periodontal input
Studies over the past 15 years have indicated that somatotopic
maps of the body can be modified by experimental
manipulations of their sensory inputs (for review, see
Merzenich et aL, 1996; Kaas, 1991). It has been found that
peripheral nerve section, digit amputation, local anesthetic
injection, behavioral experience, and task training in animals
all result in significant alterations in the organizational features
of somatosensory cortical areas. For example, behaviorally
controlled tactile stimulation of one or two digit tips in the
adult owl monkey has been shown to result in an enlargement
of the tactile sensory representation within the forelimb SI
region (Jenkins et aL, 1990). In addition, after owl monkeys
had been trained on a frequency-discrimination task, the
cortical representations of the trained hand were shown to be
spatially more complex than prior to training (Recanzone et
aL, 1992). These novel findings suggest that the details of the
representation of the body surface in somatosensory cortical
areas are modified by recent behavioral experiences.
ADV DENT RES JUNE 1999
It is possible, therefore, that after removal of periodontal
input and provision of implant-supported prostheses, plastic
changes occur in somatotopic maps in the face motor and
somatosensory cortical regions. These plastic changes may be
directly associated with the individuals' ability to
accommodate to their new prostheses. Further, the extent of
these changes, together with specific treatment differences and
individual oro-dental characteristics, may explain why some
individuals experience more difficulty than others in the
process of accommodating to either fixed or removable
prostheses. It is likely that the better the quality of the
prostheses in optimizing esthetics, form, and function, the
more readily will the sensory-motor system adapt. It follows
that the closer the final prostheses come to restoring original
function {e.g., implant-supported fixed prostheses compared
with complete dentures), the closer the sensory-motor system
will re-establish its original characteristics.
CONCLUSIONS
The importance of periodontal mechanoreception in function
and sensory discrimination is identified. Patients with implant-
supported prostheses have improved tactile discriminative
capabilities and report improved motor function in comparison
with those wearing complete dentures, although their sensory
and motor capabilities do not appear to match those of dentate
individuals. Osseoperception is defined as mechanoreception in
the absence of a functional periodontal mechanoreceptive input
but derived from temporomandibular joint (TMJ), muscle,
cutaneous, mucosal, and/or periosteal mechanoreceptors, and
which provides mechanosensory information for oral kinesthetic
sensibility in relation to jaw function and artificial tooth
contacts. In this context, both peripheral mechanoreception and
central processing of peripheral afferent information are
considered. It is apparent that, with loss of dental and
periodontal mechanoreception, other peripheral receptors
dominate in afferent projections to the sensorimotor cortex and
provide the neural basis for perceptual abilities of patients with
implant-supported prostheses. The evidence available on the
plasticity of the CNS provides a possible neural basis for our
understanding of the accommodation of patients to these
changes in dental status. However, it is also likely that an
appropriately designed implant-supported restoration, being
fixed to bone, more closely resembles the dental status before
tooth loss, and this may more appropriately restore optimal
motor and sensory function of the masticatory system.
REFERENCES
Barker D, Banks RW (1994). The muscle spindle. In:
Myology, basic and clinical. Engel AG, Franzini-Armstrong
C, editors. New York: McGraw-Hill, Inc., pp. 333-360.
Bennett MR (1997). The consciousness of muscular effort and
movement. In: The idea of consciousness. The Netherlands:
Harvard Academic, pp. 67-87.
Berry DC, Mahood M (1966). Oral stereognosis and oral ability
in relation to prosthetic treatment. Br Dent J 4:179-185.
Bonte B, Linden RWA, Scott BJJ, van Steenberghe D (1993).
VOL. 13 OSSEOPERCEPTION
Role of periodontal mechanoreceptors in evoking reflexes in
the jaw-closing muscles of the cat. J Physiol 465:581-594.
Brill N, Tryde G, Edwards C, Thomas H (1974). Age changes
in the two-point discrimination threshold in human oral
mucosa. / Oral Rehabil 1:323-333.
Byers MR, Maeda T (1997). Periodontal innervation: regional
specializations, ultrastructure, cytochemistry and tissue
interactions. Acta Med Dent Helv 2:115-133.
Capra NF, Dessem D (1992). Central connections of trigeminal
primary afferent neurons: topographical and functional
considerations. Crit Rev Oral Biol Med 4:1-52.
Carr AB, Laney WR (1987). Maximum occlusal force levels in
patients with osseointegrated oral implant prosthesis and
patients with complete dentures. Int J Oral Maxillofac Impl
2:101-108.
Chapman CE (1994). Active versus passive touch: factors
influencing the transmission of somatosensory signals to
primary somatosensory cortex. Can J Physiol Pharmacol
72:558-570.
Clark FJ, Horch KW (1986). Kinesthesia. In: Handbook of
perception and human performance. Vol. I. Sensory
processes and perception. Boff KR, Kaufman L, Thomas JP,
editors. New York: John Wiley and Sons, pp. 13-1-13-62.
Darian-Smith I (1966). Neural mechanisms of facial sensation.
Int Rev Neurobiol 9:301-395.
Darian-Smith I (1984). The sense of touch: performance and
peripheral neural processes. In: Handbook of physiology.
The nervous system. Sensory processes. Bethesda, MD:
American Physiological Society, pp. 739-788.
Dong WK, Shiwaku T, Kawakami Y, Chudler E (1993). Static
and dynamic responses of periodontal ligament
mechanoreceptors and intradental mechanoreceptors. J
Neurophysiol 69:1567-1582.
Dreyer DA, Loe PR, Metz CB, Whitsel BL (1975).
Representation of head and face in postcentral gyrus of the
macaque. J Neurophysiol 38:714-733.
Dubner R, Sessle BJ, Storey AT (1978). The neural basis of
oral and facial function. New York: Plenum Press.
Edin BB (1992). Quantitative analysis of static strain sensitivity
in human mechanoreceptors from hairy skin. J Neurophysiol
67:1105-1113.
Ferrington DG, Rowe MJ, Tarvin RPC (1987). Actions of
single sensory fibres on cat dorsal column nuclei neurones:
vibratory signalling in a one-to-one linkage. J Physiol
(Lond) 386:293-309.
Ghosh S, Murray GM, Turman AB, Rowe MJ (1994).
Corticothalamic influences on transmission of tactile
information in the ventroposterolateral thalamus of the cat:
effect of reversible inactivation of somatosensory cortical
areas I and II. Exp Brain Res 100:276-286.
Gynther BD, Vickery RM, Rowe MJ (1995). Transmission
characteristics for the 1:1 linkage between slowly adapting
type II fibers and their cuneate target neurons in cat. Exp
Brain Res 105:67-75.
Hannam AG, Matthews B (1969). Reflex jaw opening in
response to stimulation of periodontal mechanoreceptors in
the cat. Arch Oral Biol 14:415-419.
Hannam AG, Sessle BJ (1994). Temporomandibular
127
neurosensory and neuromuscular physiology. In:
Temporomandibular joint and masticatory muscle disorders.
Zarb GA, Carlsson GE, Sessle BJ, Mohl ND, editors.
Copenhagen: Munksgaard, pp. 67-100.
Haraldson T, Carlsson GE, Ingerval B (1979). Functional state,
bite force and postural muscle activity in patients with
osseointegrated oral implant bridges. Acta Odontol Scand
37:195-206.
Hammerle CHF, Wagner D, Bragger U, Lussi A, Karayiannis
A, Joss A, et al. (1995). Threshold of tactile sensitivity
perceived with dental endosseous implants and natural teeth.
Clin Oral Impl Res 6:83-90.
Huang C-S, Hiraba H, Sessle BJ (1989). Input-output
relationships of the primary face motor cortex in the monkey
(Macacafascicularis). J Neurophysiol 61:350-362.
Jacobs R, van Steenberghe D (1991). Comparative evaluation
of the oral tactile function by means of teeth or implant-
supported prostheses. Clin Oral Impl Res 2:75-80.
Jacobs R, van Steenberghe (1993). Comparison between
implant support prostheses and teeth regarding passive
threshold level. Int J Oral Maxillofac Impl 8:549-554.
Jacobs R, van Steenberghe D (1994). Role of periodontal
ligament receptors in the tactile function of teeth: a review. /
Periodont Res 29:153-167.
Jacobs R, Scholte A, van Steenberghe D (1992). Influence of
temperature and foil hardness on interocclusal tactile
threshold. J Periodont Res 27:581-587.
Jacobs R, Bou Sarhal C, van Steenberghe D (1998). The
stereognostic ability of teeth and implants (abstract). J Oral
Rehabil 25:231.
Jami L (1992). Golgi tendon organs in mammalian skeletal
muscle: functional properties and central actions. Physiol
Rev 72:623-666.
Jean A (1984). Brainstem organization of the swallowing
network. Brain Behav Evol 25:109-116.
Jenkins WM, Merzenich MM, Ochs MT, Allard T, Guic-
Robles E (1990). Functional reorganization of primary
somatosensory cortex in adult owl monkeys after
behaviorally controlled tactile stimulation. J Neurophysiol
63:82-104.
Johansson RS, Trulsson M, Olsson KA, Westberg KG (1988a).
Mechanoreceptive activity from the human face and oral
mucosa. Exp Brain Res 72:204-208.
Johansson RS, Trulsson M, Olsson KA, Abbs JH (1988b).
Mechanoreceptive afferent activity in the infraorbital nerve
in man during speech and chewing movements. Exp Brain
Res 72:209-214.
Kaas JH (1991). Plasticity of sensory and motor maps in adult
mammals. Ann Rev Neurosci 14:137-167.
Kaas JH (1996). The somatosensory cortex. In: Somesthesis
and the neurobiology of the somatosensory cortex. Franzen
O, Johansson R, Terenius L, editors. Basel: Birkhauser
Verlag,pp. 163-171.
Karayiannis AI, Lussi A, Hammerle C, Bragger U, Lang NP
(1991). Perceived pressure thresholds with natural teeth and
single crowns on osseointegrated dental implants (abstract).
J Dent Res 70(Spec Iss):460.
Kawamura Y (1983). Oral sensory mechanisms. Basel: S. Karger.
128 KUNEBERG & MURRAY
Klineberg IJ (1980). Influences of temporomandibular articular
mechanoreceptors on functional jaw movements. / Oral
Rehabil 7:307-317.
Klineberg I, Greenfield BE, Wyke BD (1971). Afferent
discharges from temporomandibular articular
mechanoreceptors. An experimental analysis of their
behavioural characteristics in the cat. Arch Oral Biol
16:1463-1479.
Lin L-D, Sessle BJ (1994). Functional properties of single
neurons in the primate face primary somatosensory cortex. El.
Modulation of responses to peripheral stimuli during trained
orofacial motor behaviors. JNeurophysiol 71:2401-2413.
Linden RWA (1990a). An update on the innervation of the
periodontal ligament. EurJ Orthod 12:91-100.
Linden RWA (1990b). Periodontal mechanoreceptors and their
functions. In: Neurophysiology of the jaws and teeth. Taylor
A, editor. Hampshire: MacMillan Press, pp. 52-95.
Linden RWA, Scott BJJ (1989a). Distribution of mesencephalic
nucleus and trigeminal ganglion mechanoreceptors in the
periodontal ligament of the cat. J Physiol 410:35-44.
Linden RWA, Scott BJJ (1989b). The effect of tooth extraction
on periodontal ligament mechanoreceptors represented in
the mesencephalic nucleus of the cat. Arch Oral Biol
34:937-941.
Lindquist LW, Carlsson GE (1986). Long-term effects on
chewing efficiency and bite force of treatment with
mandibular fixed prostheses on osseointegrated implants in
complete denture wearers. Report series 14. Lund, Sweden:
Universities of Lund and Gothenburg, Dept. of
Stomatognathic Physiology.
Lund JP (1990). Specialization of the reflexes of the jaws. In:
Neurophysiology of the jaws and teeth. Taylor A, editor.
Hampshire: MacMillan Press, pp. 142-161.
Lund JP, Matthews B (1981). Responses of temporomandibular
joint afferents recorded in Gasserian ganglion of the rabbit to
passive movements of the mandible. In: Oral-facial sensory
and motor functions. Kawamura Y, Dubner R, editors. Tokyo:
Quintessence Publishing Company, Inc., pp. 153-160.
Lund JP, Richmond FJR, Touloumis C, Patry Y, Lamarre Y
(1978). The distribution of Golgi tendon organs and muscle
spindles in masseter and temporalis muscles of the cat.
Neurosci 3:259-270.
Lundqvist S, Haraldson T (1984). Occlusal perception of
thickness in patients with bridges on osseointegrated oral
implants. Scand J Dent Res 92:88-92.
Maeda T, Byers MR (1996). Different locations of growth-
associated protein (GAP-43) in mechanoreceptors and free
nerve endings of adult rat periodontal ligament, dental pulp
and skin. Arch Histol Cytol 59:291-304.
Manger PR, Woods TM, Jones EG (1995). Representation of
the face and intraoral structures in area 3b of the squirrel
monkey {Saimiri sciureus) somatosensory cortex, with
special reference to the ipsilateral representation. J Comp
Neurol 363:597-607.
Manger PR, Woods TM, Jones EG (1996). Representation of
face and intra-oral structures in area 3b of macaque monkey
somatosensory cortex. J Comp Neurol 371:513-521.
Mantecchini G, Bassi F, Pera P, Preti G (1998). Oral
ADV DENT RES JUNE 1999
stereognosis in edentulous subjects rehabilitated with
complete removable dentures. J Oral Rehabil 25:185-198.
Matthews PBC (1988). Proprioceptors and their contribution to
somatosensory mapping: complex messages require
complex processing. Can J Physiol Pharmacol 66:430-438.
McClean MD, Dostrovsky JO, Lee L, Tasker RR (1990).
Somatosensory neurons in human thalamus respond to
speech-induced orofacial movements. Brain Res 513:343-347.
McCloskey DI (1978). Kinesthetic sensibility. Physiol Rev
58:763-820.
McCloskey DI (1981). Corollary discharges: motor commands
and perception. In: Handbook of physiology. The nervous
system. Vol. II. Motor control. Brooks VB, editor. Bethesda,
MD: American Physiological Society, pp. 1415-1480.
Merzenich MM, Wang X, Xerri C, Nudo R (1996). Functional
plasticity of cortical representations of the hand. In:
Somesthesis and the neurobiology of the somatosensory
cortex. Franzen O, Johansson R, Terenius L, editors. Basel:
Birkhauser Verlag, pp. 249-269.
Morimoto T (1990). Perception of intraoral stimulation. In:
Neurophysiology of the jaws and teeth. Taylor A, editor.
Hampshire: MacMillan Press, pp. 369-390.
Mountcastle VB (1984). Central mechanisms in
mechanoreceptive sensibility. In: Handbook of physiology.
The nervous system. Sensory processes. Bethesda, MD:
American Physiological Society, pp. 789-878.
Miihlbradt L, Ulrick R, Muhlemann H, Schmid H (1989).
Mechanoperception of natural teeth versus endosseous
implants revealed by magnitude estimation. Int J Oral
Maxillofac Impl 4:125-130.
Murray GM, Sessle BJ (1992a). Functional properties of single
neurons in the face primary motor cortex of the primate. I.
Input and output features of tongue motor cortex. J
Neurophysiol 67:747-758.
Murray GM, Sessle BJ (1992b). Functional properties of single
neurons in the face primary motor cortex of the primate. II.
Relations with trained orofacial behavior. / Neurophysiol
67:759-774.
Penfield W, Rasmussen T (1950). The cerebral cortex of man.
New York: MacMillan.
Proske U (1981). The Golgi tendon organ. Properties of the
receptor and reflex action of impulses arising from tendon
organs. In: Neurophysiology IV. International Review of
Physiology. Vol. 25. Porter R, editor. Baltimore, MD:
University Park Press, pp. 127-171.
Proske U, Schaible H-G, Schmidt RF (1988). Joint receptors
and kinesthesia. Exp Brain Res 72:219-224.
Recanzone GH, Merzenich MM, Jenkins WM, Grajski KA,
Dinse HR (1992). Topographic reorganization of the hand
representation in cortical area 3b of owl monkeys trained in a
frequency-discrimination task. J Neurophysiol 67:1031-1056.
Rossignol S, Lund JP, Drew T (1988). The role of sensory
inputs in regulating patterns of rhythmical movements in
higher vertebrates. In: Neural control of rhythmic
movements in vertebrates. Cohen A, Rossignol S, Grillner S,
editors. New York: John Wiley & Sons, pp. 201-283.
Rowe MJ, Turman AB, Murray GM, Zhang HQ (1996).
Parallel organization of somatosensory cortical areas I and II
VOL.13
for tactile processing. Clin Exp Pharm Physiol 23:931-938.
Sakada S (1983). Physiology of mechanical senses of the oral
structure. In: Frontiers of oral physiology. Vol. 4. Oral
sensory mechanisms. Kawamura Y, editor. Basel: S. Karger,
pp. 1-32.
Siirila HS, Laine P (1972). Sensory threshold in
discriminating differences in thickness between the teeth
by different degrees of mouth opening. Proc Finn Dent Soc
68:134-139.
Tabata T, Suzuki T, Watanabe M (1995). Response
characteristics of periodontal mechanoreceptors to
mechanical stimulation of canine and incisor teeth in the cat.
Arch Oral Biol 40:873-878.
Thilander B (1961). Innervation of the temporo-mandibular
joint capsule in man. Trans R Sch Dent Umed 7:1-67.
Trulsson M, Johansson RS (1996). Encoding of tooth loads by
human periodontal afferents and their role in jaw motor
control. Proj Neurobiol 49:267-284.
OSSEOPERCEPTION 129
Trulsson M, Johansson RS, Olsson KA (1992). Directional
sensitivity of human periodontal mechanoreceptive afferents
to forces applied to the teeth. / Physiol 447:373-389.
Turker KS, Yang J, Brodin P (1997). Conditions for excitatory
or inhibitory masseteric reflexes elicited by tooth pressure in
man. Arch Oral Biol 42:121-128.
Vickery RM, Gynther BD, Rowe MJ (1994). Synaptic
transmission between single slowly adapting type I fibres
and their cuneate target neurones in cat. J Physiol (Lond)
474:379-392.
Wiesendanger M, Miles TS (1982). Ascending pathway of
low-threshold muscle afferents to the cerebral cortex and its
possible role in motor control. Physiol Rev 62:1234-1270.
Woolsey CN, Settlage PH, Meyer D, Sencer W, Hamuy TP,
Travis AM (1952). Patterns of localization in precentral and
"supplementary motor areas" and their relation to the
concept of a premotor area. Bard P, editor. Baltimore, MD:
The Williams & Wilkins Company, pp. 238-264.