sensorio motor

Review Article

Sensory-motor function of human periodontal

mechanoreceptors*

M. TRULSSON Institute of Odontology, Karolinska Institutet, Huddinge, Sweden

SUMMARY Natural teeth are equipped with perio-

dontal mechanoreceptors that signal information

about tooth loads. In the present review, the basic

force-encoding properties of human periodontal

receptors will be presented along with a discussion

about their likely functional role in the control of

human mastication. Microneurographic recordings

from single nerve fibres reveal that human perio-

dontal receptors adapt slowly to maintained tooth

loads. Most receptors are broadly tuned to the

direction of force application, and about half re-

spond to forces applied to more than one tooth.

Populations of periodontal receptors, nevertheless,

reliably encode information about both the teeth

stimulated, and the direction of forces applied to

the individual teeth. Information about the magni-

tude of tooth loads is made available in the mean

firing rate response of periodontal receptors. Most

receptors exhibit a markedly curved relationship

between discharge rate and force amplitude, featur-

ing the highest sensitivity to changes in tooth load at

very low force levels (below 1 N for anterior teeth

and 4 N for posterior teeth). Thus, periodontal

receptors efficiently encode tooth load when sub-

jects contact and gently manipulate food using the

teeth. It is demonstrated that signals from perio-

dontal receptors are used in the fine motor control

of the jaw and it is clear from studies of various

patient groups (e.g. patients with dental implants)

that important sensory-motor functions are lost or

impaired when these receptors are removed during

the extraction of teeth.

KEYWORDS: mechanoreceptor, microneurography,

sensory-motor control, tooth, implant, mastication

Accepted for publication 27 January 2006

Introduction

To control oral motor behaviours such as biting, chew-

ing, speech and oral manipulation, the brain relies on

information from sense organs in the orofacial struc-

tures (1–3). Natural teeth are equipped with extremely

sensitive tactile sensors – periodontal mechanoreceptors

(2, 4, 5). These sensors provide information about tooth

loads and are located among the collagen fibres in the

ligaments that attach the root of the tooth to the alveolar

bone. If we are to understand how periodontal receptors

contribute to the control of oral motor behaviours, a

description of the information they carry to the brain

during these behaviours is essential. With this know-

ledge, it is possible to formulate and test hypotheses on

the likely functional role of periodontal receptors. Solid

knowledge on how the brain utilizes sensory signals to

regulate oral motor behaviours is a prerequisite for

understanding the functional consequences of many

clinical treatments. For example, when a natural tooth

is replaced by a dental implant the periodontal ligament

disappears and the information from periodontal recep-

tors about tooth loads is no longer available for the

regulation of oral motor functions. In this review, the

basic force-encoding properties of human periodontal

receptors including a description of their signalling

during biting and chewing will be presented and

discussed in the light of their likely functional role in

the control of oral motor actions. The functional

consequences of replacing natural teeth with oral

implants will also be commented on.

*Based on the Journal of Oral Rehabilitation Summer School 2005 in

Bevagna, Italy. Kindly sponsored by Blackwell Munksgaard and Nobel

Biocare.

ª 2006 Blackwell Publishing Ltd doi: 10.1111/j.1365-2842.2006.01629.x

Journal of Oral Rehabilitation 2006 33; 262–273

Recording signals from human periodontalreceptors

Nerve signals were recorded from single periodontal

afferents innervating anterior and posterior teeth in

healthy adult volunteers. The neural data were

obtained by the microneurographic technique devel-

oped by Vallbo and Hagbarth (6). The inferior alveolar

nerve was approached through the oral cavity and

impaled by a tungsten needle electrode near its

entrance at the mandibular foramen (Fig. 1a) (7, 8).

Manual handling of the electrode was guided by

landmarks used in dental practice when blocking the

mandibular nerve. Once the tip of the electrode was

located in a nerve fascicle, its position was carefully

adjusted until impulse responses from a single afferent

were obtained. The electrode was then left undisturbed

in this recording position, supported only by the

surrounding tissues.

To activate periodontal receptors during the search

for single-unit responses, light mechanical stimuli

(<5 N) were applied manually to the crowns of the

teeth. The search strategy adopted in these experiments

was optimized for low-threshold mechanoreceptive

afferents. Thus, other types of afferents that may

contribute to dental mechanosensitivity (e.g. high-

threshold periodontal afferents and intra-dental affer-

ents) were not studied and will not be further discussed

(e.g. see Ref. 9).

When stable recordings were obtained from single

periodontal afferents, controlled forces were applied to

small nylon cubes cemented to the incisal edges or

occlusal surfaces on individual teeth. The neural

discharge was recorded in response to forces applied

in four directions in the horizontal plane (lingual,

facial, mesial, distal) and in the two axial directions

(up and down; Fig. 1b). Recordings from the inferior

alveolar nerve revealed that human periodontal

mechanoreceptors discharge continuously during sus-

tained loading of the teeth. However, consistent with

animal studies (see Refs 4, 5), it was found that the

receptors’ slow-adapting nature might not be recog-

nized if the stimuli are limited to directions of

application that activate the receptors poorly. Like

the slow-adapting type II (SA II) mechanoreceptors in

the skin, most human periodontal mechanoreceptors

(about 70%) are active spontaneously and discharge

regularly in response to forces applied to the teeth

(Fig. 2a).

Receptor encoding of spatial aspects oftooth loads

Typically, periodontal mechanoreceptors are broadly

tuned to the direction of tooth loading (Fig. 2). That is,

the afferents normally respond to forces applied to the

receptor-bearing tooth in two to four of the six test

directions (8, 10). These receptive field properties are in

concordance with those observed in the cat, but are in

contrast to those in the dog, which appeared to have

narrower receptive fields (11–13). As a result of the

broad directional tuning, an individual periodontal

(a)

(b)

Fig. 1. (a)Recording from periodontal mechanoreceptors in the

inferior alveolar nerve in man. Forces are applied to the central

incisor by the use of a hand-held probe equipped with force

transducers (FT) for continuous force measurement. Note the small

nylon sphere at the end of the probe and the nylon cubes attached

to the teeth. (b) A tooth is shown in the horizontal plane (left) and

in a vertical plane (right). Each of the six directions of stimulation

are represented by the arrows: Fa, Me, Li, Di, Do and Up refer to

facial, mesial, lingual, distal, downward and upward, respectively.

The forces were applied to each of the five free faces on the nylon

cube cemented to the tooth just above its edge. The probe slipped

off the cube if the force was not applied perpendicular to the faces,

ensuring that data were collected only in the desired direction of

force application. The upward force (Up) was applied with a nylon

loop (not shown) [Reprinted from Progress in Neurobiology, Vol.

49 Trulsson M, Johansson RS. Encoding of tooth loads by human

periodontal afferents and their role in jaw motor control pp 267–

284, Copyright 1996, with permission from Elsevier].

S E N S O R Y - M O T O R F U N C T I O N O F H U M A N P E R I O D O N T A L M E C H A N O R E C E P T O R S 263

ª 2006 Blackwell Publishing Ltd, Journal of Oral Rehabilitation 33; 262–273

mechanoreceptor provides ambiguous information

about the direction of force applied to the tooth.

However, analyses based on vector calculations show

that information about the precise direction of force is

represented reliably in the activity from small popula-

tions of periodontal mechanoreceptors (8).

The receptive field of human periodontal mecha-

noreceptors often extends beyond a single tooth. About

half of the periodontal mechanoreceptors respond to

loading of groups of adjacent teeth, typically two to four

teeth (10, 14). Each afferent always exhibits the highest

response rates to stimulation of one particular tooth,

the so-called receptor-bearing tooth, with a gradual and

rather sharp decline in responsiveness to loads applied

to the adjacent teeth (Fig. 3). Moreover, the preferred

directions of the different teeth strongly suggest that

multi-tooth receptive fields result from mechanical

coupling between neighbouring teeth by interdental

contacts and trans-septal collagen fibres, rather than by

branching of axons to more than one tooth.

The multiple-tooth characteristics of the receptive

fields imply that during mastication not only are the

periodontal afferents that innervate the tooth to which

a force is directly applied activated, but so are those that

innervate the adjacent teeth. However, considering the

rather sharp decline in both number of activated

afferents and response intensities from the receptor-

bearing tooth to the adjacent teeth, we hypothesized

that the population of human periodontal afferents

accurately encodes the location of the tooth directly

loaded. By the use of artificial neural networks it was

shown that the population response in human perio-

dontal afferents indeed contains detailed information

about both the direction of applied forces and the tooth

loaded (15). Thus, the existence of multiple-tooth recep-

tive fields does not downgrade the ability of the central

nervous system to uniquely locate a force stimulus

striking a particular tooth. Overlapping peripheral

receptive fields are characteristic of all sensory systems

and have been shown to improve, rather than degrade,

their spatial localization and resolution (e.g. 16).

Periodontal receptors of anterior and posterior teeth

do indeed demonstrate similarities but there are also

some important differences (10, 17). The use of vector

calculations to identify differences in the periodontal

receptors at different types of teeth is illustrated in

Fig. 4. Based on the receptors’ response to forces

applied in each of the six test directions, its single

Fig. 2. Directional sensitivity of human periodontal receptors. (a–b) Responses of a single periodontal receptor to forces applied in six

directions to the lower central incisor (the receptor-bearing tooth). (a) Examples of nerve recordings with the corresponding force records

above each. (b–f) Vectorial representation of the responses for five afferents to sustained force application in the horizontal (left) and axial

(right) directions. (b illustrates the afferent shown in a). The length of each vector is proportional to the mean discharge rate evoked in

each direction. The spontaneous discharge rate is represented by the circle with the radius indicating its intensity. Vectors longer and

shorter than this radius illustrate increased and decreased firing, respectively. The thick arrow represents an estimate of the most efficient

excitatory stimulus direction in the horizontal plane, i.e. the calculated preferred direction [Reprinted from the Journal of Physiology-

London, Vol. 447, Trulsson M, Johansson RS, Olsson KA. Directional sensitivity of human periodontal mechanoreceptive afferents to

forces applied to the teeth, pp 373–389, Copyright 1992, with permission from Blackwell Publishing].

M . T R U L S S O N264


‘preferred direction’ was calculated by vector summa-

tion (see the thick arrows in Fig. 2b–f). The vectors in

Fig. 4 represent the preferred directions for all perio-

dontal receptors that have been studied in man. Each

cluster of arrows represents the vectors calculated for all

of the receptors that were examined in all teeth of that

type (anterior teeth, first premolars, the second pre-

molars and the first molars).

Note that the number of vectors decreases from the

anterior teeth to the molar, indicating a decreasing

number of receptors in the periodontal ligaments

distally along the dental arch. This finding is supported

by several histological studies (18–20) and attests to the

importance of a well-developed mechanoreceptive

innervation of the anterior part of the mouth. When

food is taken into the mouth, the morsel will be split

into smaller pieces by the front teeth before it is moved

to posterior parts of the dentition. Sometimes, the front

teeth are even used as a ‘third hand’ in manipulative

tasks, or as a precision cutting tool. Proper execution of

such tasks relies heavily on sensory information as

those involving execution of comparable manipulative

tasks performed by the densely innervated fingertips of

the hand (21).

In the horizontal plane, the preferred directions of

the receptors supplying the anterior teeth and the

premolars are quite evenly distributed around the

circumference of the tooth (Fig. 4). The receptors

supplying the molars, however, have a clear preference

for the distal-lingual direction. In the vertical plane,

there is a preference for downward-directed forces, but

with fewer receptors responding preferentially in this

direction with distance along the arch.

The shift from a high sensitivity to most directions at

the anterior teeth to the distal-lingual direction at the

molars meets the functional demands of the anterior

versus posterior teeth. When the anterior teeth are

manipulating food morsels and splitting them into

pieces in the initial stages of food intake, forces are

Fig. 4. Preferred directions of individual receptors of different

teeth projected to the horizontal plane and two vertical planes,

respectively [Reprinted from the Journal of Physiology-London,

Vol. 447, Trulsson M, Johansson RS, Olsson KA. Directional

sensitivity of human periodontal mechanoreceptive afferents to

forces applied to the teeth, pp 373–389, Copyright 1992, with

permission from Blackwell Publishing].

Fig. 3. Receptive field of a single periodontal mechanoreceptor

showing steady-state responses to maintained mechanical stimu-

lation of five teeth, illustrated from a horizontal view (a) and a

facial view (b). The vectors illustrate the receptor’s response to a

tooth load of 250 mN. The tested teeth: c1 ¼ contralateral central

incisor, 1 ¼ central incisor, 2 ¼ lateral incisor, 3 ¼ canine,

4 ¼ first premolar. RBT, receptor-bearing tooth [Reprinted from

the Journal of Neurophysiology, Vol. 69, Trulsson M. Multiple –

tooth receptive fields of single human periodontal mechano

receptive afferents, pp 474–481, Copyright 1993, with permission

from the American Physiological Society].



applied to them in all directions. The molars, on the

other hand, grind food substances only during more

forceful chewing. During the final phase of the chewing

cycle, when the lower molars on the working side

approach the intercuspal position from a posterior and

lateral position, they are likely to experience distal and

lingually directed forces upon contact with the oppo-

sing upper molar teeth. Studies on tooth displacement

during oral function indicate a tilt of the first molar

during chewing and biting in a lingual direction (22,

23). Given their directional preference for distal-lingual

loading, the mechanoreceptors supplying the lower

molar teeth are well suited to encode information about

the forces that normally act on the posterior teeth

during mastication.

Receptor encoding of intensive aspects oftooth loads

To study the encoding of intensity of tooth loads by

human periodontal receptors, ramp-and-hold-shaped

force profiles were delivered to the receptor-bearing

tooth in its most responsive direction (Fig. 5a) (17, 24).

The relationships between the magnitude of the sus-

tained force and the steady-state discharge rate for a

group of periodontal receptors supplying the anterior

Fig. 5. (a–b) Responses of human periodontal mechanoreceptors to sustained forces of various amplitudes applied to the receptor-bearing

tooth (an incisor or a canine) in the most responsive direction. (a) Examples of force stimulation and nerve recordings of a single afferent

during stimuli of four different amplitudes. (b) Stimulus–response functions for 19 periodontal receptors. The curves fitted to the data are

defined by the function F/(F + c), where F represents the force, and c the force at which half the estimated maximum discharge rate is

attained. Solid and dashed curves refer to afferents showing saturating stimulus–response relationships (n ¼ 15) and non-saturating

relationships (n ¼ 4), respectively. The curve labelled ‘a’ refers to the same afferent as illustrated in (a). (c) Responses of a saturating and a

non-saturating receptor to an abrupt increment in force superimposed on a sustained force [Reprinted from the Journal of

Neurophysiology, Vol. 72, Trulsson M, Johansson RS. Encoding of amplitude and rate of forces applied to the teeth by human periodontal

mechanorecetive afferents, pp 1734–1744, Copyright 1994, with permission from the American Physiological Society.



teeth are shown in Fig. 5b. For each periodontal

afferent investigated, the steady-state discharge rate

was approximately proportional to F/(F + c), where ‘F’

represents the force, and ‘c’ the force at which half the

estimated maximum discharge rate is attained. This

transform implies that the discharge rate increases more

or less linearly until F approaches c and then levels off.

Similar stimulus–response relationships were observed

in less-responsive directions of stimulation, but with

lower discharge rates. These stimulus–response relation-

ships characterize the static sensitivities of the receptors

to different forces applied to the teeth. The solid curves in

Fig. 5b show that the response to a continuous force is a

markedly downward-curved or hyperbolic relationship

(see solid curves in figure) for most of the human

periodontal mechanoreceptors (about 80%). The slopes

of the curves are steepest between 0 and 1 N, which

indicates that these receptors are most sensitive to

changes in sustained force levels below about 1 N in

magnitude. In contrast to the steeply inclined nature of

the curves below these limits, the curves are almost

horizontal for sustained force levels above the limits. This

indicates that the individual afferents signal the presence

of higher forces but provide the brain with no useful

information as to their magnitudes. That is, the discharge

of each afferent saturates and attains approximately its

highest rate for all force levels above the limit. Saturating

stimulus–response relationships similar to those of most

human periodontal receptors are also characteristic of

periodontal receptors in animal studies (25–28).

In addition to their sensitivity to static forces, peri-

odontal receptors are also sensitive to rapidly changing

forces. Their sensitivity to rapidly changing forces, or

dynamic sensitivity, varies in parallel with their sensi-

tivity to slow changes in static force. This is illustrated

for a saturating receptor on the left of Fig. 5c. After

approximately 1.5 s of exposure to a sustained force,

the tooth was further loaded with a rapid increment in

force. The rapid increase in force evoked an increase in

the steady-state discharge rate that was less than the

addition evoked by the much smaller increment at the

onset of the sustained force. That is, despite the fact that

this force increment was larger and applied at a higher

rate, the receptor discharged more strongly to the

smaller increment in force and lower force rate at the

initial contact with the tooth. This is due to saturating

receptors becoming progressively less sensitive to both

the magnitude and rate of rapid changes in force, as

contact force grows in amplitude.

In contrast to the majority of human periodontal

mechanoreceptors whose responses saturate at very

low forces, a minority (about 20%) do not saturate over

the same range of forces. These non-saturating recep-

tors exhibit stimulus–response relationships that are

nearly linear (see dotted curves in Fig. 5b). The non-

saturating receptors efficiently encode changes in static

force also at high force levels. As for the saturating

afferents, the dynamic sensitivity of the non-saturating

afferent parallels its static sensitivity. Thus, sensitivity to

rapid changes in force is maintained at high force levels.

This is illustrated for a non-saturating afferent to the

right in Fig. 5c. The strong discharge evoked by the

terminal, rapid increment in force was by far the largest

component of the afferent’s total response to the

stimulation.

The general shape of the steady-state stimulus–

response relationships is similar for periodontal recep-

tors at anterior and posterior teeth (17, 24). For both

posterior (85%) and anterior teeth (about 80%) a

majority of the receptors show a strongly saturating

stimulus–response relationship. However, compared

with receptors associated with anterior teeth, the

receptors at posterior teeth demonstrate a lower sensi-

tivity at low force levels. Figure 6 illustrates this by the

Fig. 6. Mean value of all steady-state stimulus–response func-

tions for receptors at the posterior (grey curves; n ¼ 20) and

anterior teeth (black curves; n ¼ 19), respectively. The solid and

dashed lines represent the mean � 1 s.d. of the stimulus–response

functions. Note the steeper curve at low force levels for the

receptors at anterior teeth indicating a higher sensitivity at low

forces compared with the receptors at posterior teeth [Reprinted

from the Journal of Neurophysiology, Vol. 93, Johnsen SE,

Trulsson M. Encoding of amplitude and rate of tooth loads by

human periodontal afferents from premolar and molar teeth,

pp 1889–1897, Copyright 2005, with permission from the Amer-

ican Physiological Society].



steeper average stimulus response curve for receptors at

anterior (grey curve) than at posterior teeth (black

curve). Furthermore, the dynamic sensitivity is both

lower and slower for the posterior receptors. The lower

static and dynamic sensitivity of periodontal receptors

at posterior teeth may reflect a functional adaptation to

the faster and stronger forces that are developed during

motor activities involving the posterior teeth.

Receptor encoding of tooth loads duringbiting and chewing

In order to understand how periodontal receptors

contribute to the control of oral motor behaviours such

as biting and chewing, a description of the information

they carry to the brain during these behaviours is

essential. For technical reasons, intraoral recordings are

not easily made from human periodontal afferents

during oral motor functions. Thus, to be able to describe

the responses of human periodontal receptors to arbi-

trary load profiles, a quantitative model has been

developed that successfully incorporates both the static

and dynamic sensitivity of the receptors (17, 24). In this

model, the discharge rate of a receptor is the weighted

sum of a static response component derived from the

F/(F + c) transform and a dynamic response component

derived from a high-pass filtering of the same trans-

form. The model parameters (weight factors, time

constants of the filter, etc.) are characteristic for each

individual receptor. The results of the modelled dis-

charge rates turned out to be practically identical as

those actually measured for novel force stimulations,

i.e., stimuli that were not included during the devel-

opment of the model (for further details see Ref. 24).

To predict the receptor discharge evoked by biting

with the anterior teeth, the subject was instructed to

manipulate and bite through a morsel of food resting on

a bar equipped with force transducers (Fig. 7a) (29, 30).

The forces that were developed between the incisors

when cracking a peanut (during a single-phase ‘split

task’) and when first holding it briefly between the

teeth (during a two phase ‘hold-and-split task’) are

shown in the top panels of Fig. 7b and c, respectively.

Below each force recording is shown the predicted

discharge rates from two periodontal receptors, one

saturating and one non-saturating receptor.

The model predicted that the saturating receptor

would respond distinctly to the small force produced

by the initial contact with the peanut, and would provide

an on-going response when the subject held the peanut

between the teeth (hold phase). Thereby, signalling

information about small changes in force and low levels

of sustained force. However, during rapid exertion of the

higher forces required to split the peanut (split phase),

(a) (b) (c)

Fig. 7. Simulated periodontal receptor responses to empirically recorded force traces (shown at the top) during a ‘split’ task (b) and a

‘hold-and-split’ task (c) with a peanut. The apparatus used to record the force profiles exerted on the food is shown in (a). Subjects were

instructed to position the bar so that the food morsel could be held and split by a pair of opposing central incisors. The food morsel rested

on a horizontal plate of duraluminum equipped with force transducers (FT) for force measurement. Below the force traces in (b) and (c)

are shown simulated receptor responses of a typical saturating and non-saturating anterior periodontal receptor. Note that the two types of

periodontal receptors select out and signal different aspects of the forces generated during the behavioural tasks [Reprinted from Progress

in Neurobiology, Vol. 49, Trulsson M, Johansson RS. Encoding of tooth loads by human periodontal afferents and their role in jaw motor

control, pp 267–284, Copyright 1996, with permission from Elsevier].



the receptor exhibited only a moderate and declining

discharge rate. It is noteworthy that the highest dis-

charge rates occurred in response to the initial low force

levels at tooth contact and not to the higher amplitudes

or force rates exerted during the split phase.

In contrast, the non-saturating receptor is predicted

by the model to encode information about force

throughout the split phase. As dynamic sensitivity

parallels static sensitivity, the small forces at the initial

contact with the peanut and during the hold phase

resulted in much lower discharge rates than for the

substantially higher forces generated during the split

phase. However, due to the receptor’s dynamic sensi-

tivity at high force levels, its discharge rates were

predicted to provide a distorted reflection of the forces

during the split phase. Figure 7c shows that the rate of

force recruitment was momentarily slowed during the

split phase, which resulted in a ‘notch’ in the discharge

profile rather than two distinct levels of firing.

While the anterior teeth are used during initial food

intake, when morsels are manipulated, split into smal-

ler pieces and transported into the mouth, the posterior

teeth are used during rhythmical chewing when strong

forces are produced by the jaw muscles to grind the

food. During normal chewing of mixed food the forces

exerted on one posterior tooth rarely exceed 50–70 N

(31). To predict the discharge from periodontal recep-

tors at posterior teeth evoked during chewing, the

subject was instructed to ‘chew’ on a force transducer

placed between a pair of molars (17). The chewing

forces that were developed between the molars are

shown in the top panel of Fig. 8. Below the force trace

is the predicted discharge rates from two posterior

periodontal receptors, one saturating and one non-

saturating receptor.

The simulations of periodontal receptor responses to

chewing-like force profiles predict that the discharge

rates of the saturating receptors rapidly increase at

initial tooth contact. The receptors continue to dis-

charge as long as the tooth is loaded, but because of the

marked saturation tendencies at higher forces these

receptors poorly encode the magnitude of the strong

chewing forces and the force changes occurring at these

high loads (see the saturating receptor in Fig. 8). The

saturating receptors show their highest discharge rates

shortly after the initial tooth contact and the discharge

rates decrease to a saturated level even if the force

continues to increase. Indeed, response saturation of

the periodontal afferents have been described in

anaesthetized rabbits while chewing on a rubber tube

(32). However, the non-saturating receptors constitu-

ted a subpopulation of periodontal receptors that

encoded forces over a wide intensity range (see the

non-saturating receptor in Fig. 8), including forces

developed during the power phase of chewing (31).

Taken together, these observations from the model

simulations demonstrate that periodontal receptors

possess the capacity to signal information about the

mechanical events that occur when humans manipu-

late and bite food with their anterior teeth and chew

food with their posterior teeth. Receptors with different

force-encoding characteristics capture and emphasize

different aspects of the mechanical events in their

discharge. The simulations suggest that the saturating

and the non-saturating periodontal receptors exhibit

diverse sensory functions during mastication.

Role of periodontal receptors in jaw motorcontrol

Motor activity for mastication can be generated by

neuronal networks in the brain stem in the absence of

sensory information from the mouth and face (for

review see Ref. 1). However, signals from mechanore-

ceptors are required for an efficient and adaptive

execution of the masticatory sequence, i.e. from the

acceptance of food to swallowing. As the periodontal

Fig. 8. Simulated periodontal receptor responses to force profiles

recorded during ‘chewing’ on a force transducer placed between a

pair of molars. Ten different chewing-like force profiles with peak

forces ranging from 3 to 52 N are shown at the top. Below the

force traces, simulated receptor responses are shown for a typical

saturating and a non-saturating posterior periodontal receptor.

Just like the anterior periodontal receptors, the two types of

posterior receptors signal different aspects of the forces acting on

the teeth during normal function [Reprinted from the Journal of

Neurophysiology, Vol. 93, Johnsen SE, Trulsson M. Encoding of

amplitude and rate of tooth loads by human periodontal afferents

from premolar and molar teeth, pp 1889–1897, Copyright 2005,

with pemission from the American Physiological Society].



mechanoreceptors encode information about the tem-

poral, spatial and intensive aspects of tooth loads, it is

likely that their inputs contribute to the regulation of

the muscle activity that generates masticatory forces

and jaw movements. Indeed, there are several investi-

gations, both in animals and man, indicating that

periodontal receptors are involved in the control of

the jaw muscles during biting and chewing (see Refs 1,

2). For a comprehensive account of the inhibitory and

excitatory reflex responses that may be evoked in the

jaw-closing muscles in humans when periodontal

receptors are stimulated, the reader is referred to the

excellent review by Turker (3).

As a large majority of the periodontal receptors

innervating the anterior teeth are highly sensitive to

forces and changes in force levels of <1 N, it was

hypothesized that their input is used for the regulation

of precise manipulative actions involving application of

low forces by the jaw (29). The ‘hold-and-split’ task

described above simulates the natural situation of

positioning and holding food between the teeth prior

to biting and provided a means to evaluate this

hypothesis. Three separate observations suggest that

subjects do use periodontal mechanoreceptive informa-

tion to regulate the level of jaw force during the hold

phase of the ‘hold-and-split’ task (Fig. 9a). First, the

distribution of hold forces coincide over the range at

which periodontal receptors are most sensitive to

changes in force (Fig. 9c). That is, subjects choose to

use hold forces large enough to achieve a stable clasp

(on average 0.6 N), but automatically avoid higher

forces (>1 N) at which the sensitivity of most receptors

(the saturating receptors) to force changes is compro-

mised. Secondly, during anaesthesia of the periodontal

tissues, the hold forces are considerably increased and

show greater variability, both during the individual

trials and between trials (Fig. 9c; also compare the force

profiles in Fig. 9a and b) (29). Finally, patients lacking

periodontal receptors, such as patients using dental

prostheses supported by the oral mucosa or dental

implants (Fig. 9d) showed similarly high hold force

levels (33). These higher hold forces provided a greater

0·5 s 0·5 s

10 N

Hold-and-splitpeanut

Normal periodontal sensibility

Hold-and-splitpeanut

Anesthesia of the periodontium

10 N

10

20

30

0

10

20

Fre

quen

cy o

f tria

ls (

%)

0 Sta

tic s

ensi

tivity

imp

s–1 N

–1

0 1Hold force (N)

2 3 4

Normal, hold-and-split trialsAnesthesia, hold-and-split trials

0

1

2

3

4

Hol

d fo

rce

(N)

Nat Imp Nor AneDen

(a)

(c)

(b)

(d)

Fig. 9. (a, b) Examples of force profiles (five superimposed trials) obtained during the hold-and-split task with peanuts during normal

periodontal sensibility and during anaesthesia of the periodontium, respectively. Note, the considerably higher and more variable hold

forces produced by the subjects during the periodontal anaesthesia. (c) Frequency distribution of hold forces spontaneously adopted by the

subjects; solid and dashed line histograms refer to trials with normal sensibility and trials with anaesthesia of the periodontium,

respectively. Superimposed curves represent the sensitivity to changes in tooth load of human periodontal afferents. The three dotted

curves refer to the mean � 1 s.d. of the first force differential averaged across the 19 periodontal afferents in Fig. 5b. (From Trulsson M,

Johansson RS: Exp Brain Res 107: 486–496, 1996.) (d) The left histogram shows the mean hold forces employed by subjects in the natural

(Nat), denture (Den) and implant (Imp) groups. Average values for individual subjects are indicated by filled circles (n ¼ 20). Right bar

histograms represent the mean hold force by subjects during normal conditions (Nor) and during periodontal anaesthesia (Ane). Vertical

lines represent the range of average values for individual subjects [Reprinted from the Journal of Dental Research, Trulsson M, Gunne

HSJ. Food-holding and -biting behavior in human subjects lacking periodontal receptors, pp 574-582, Copyright 1998, with permission

from the international and American Associations for Dental Research].



level of security in maintaining the clasp on the morsel

and probably stimulate alternative, less sensitive mech-

anoreceptors in the tissues that are able to signal its

engagement by the teeth. Furthermore, in anaesthe-

tised subjects, and in patients lacking periodontal

receptors, the morsel frequently escaped from the

incisal edges during the biting task, indicating an

impaired spatial control of the jaw-action vector

(29, 33). Thus, when periodontal afferent information

is lacking, patients show a marked disturbance in the

control of precisely directed, low biting forces, suggest-

ing that periodontal receptors play an important role in

the specification of the level, direction and point of

attack of forces used to hold and manipulate food

between the teeth.

To efficiently handle food during chewing, activation

of the jaw muscles must be coordinated to produce jaw

actions that are spatially adapted to the food’s distribu-

tion in relation to the teeth. During strong chewing

forces, most of the periodontal receptors are saturated

and poorly encode the magnitude of tooth loads (17).

However, the receptor responses are still dependent on

the direction of the force (10, 24). Thus, during chewing,

the periodontal receptors continuously encode spatial

information about tooth loads and most likely contrib-

ute to the spatial control of jaw actions. Indeed, lack of

coordination in chewing has been observed following

denervation of intraoral receptors including periodontal

receptors. The absence of sensory input resulted in

reduced masticatory force and distorted spatial control

of jaw movements during chewing (34, 35).

Given their high sensitivity at low forces, most

periodontal receptors are particularly well suited to

encode in detail the temporal changes in the chewing

force that occur during the early contact phase of each

chewing cycle. From this information, and information

about the movement of the jaw, the mechanical

properties of the food can be derived. Accordingly,

signals from the periodontal receptors may contribute

to the selection of the most appropriate motor signals,

given the existent mechanical food properties. This

would take place in a predictive feed-forward manner

based on learned relationships between patterns of

receptor signals and appropriate efferent signals (cf. 36).

The hypothetical function of early ‘state information’

in the control of forthcoming jaw actions brings to mind

that served by tactile receptors in the human fingertips

during grasping and manipulation of small objects.

Immediately following contact with an object, tactile

receptors encode various mechanical contact provisions

including information about the frictional characteris-

tics of the object (36, 37). Such information is used to

trigger the release of motor commands for subsequent

phases of manipulative manoeuvres and to predictively

modify the force output to the physical properties of the

object (38).

These principles are also expressed in the control of

chewing. Ottenhoff et al. (39, 40) have shown that the

‘additional muscle activity’ (AMA) required during the

power phase to overcome the impedance of the food is

largely parameterised in advance on the basis of sensory

experiences during the preceding chewing cycle. Mem-

ory of the food’s resistance in the previous cycle is used

to predictively scale the muscle commands that initiate

the power phase. It is also used to regulate the strength

of a sensory mediated ‘reflex’ increase in muscle

activity elicited by contact with the food resistance; a

maximum output strength of the ‘reflex’ contribution

to the AMA is set (40). Signals from periodontal

receptors may contribute both to information about

the food resistance gained during the previous cycle,

and to the ‘reflex’ mediated component of the AMA

(40).

Studies on anaesthetized rabbits performing rhyth-

mical jaw movements confirm that the AMA often

precedes the tooth contact, supporting the operation of

a feed-forward control mechanism (41). Blocking of the

periodontal receptor input did not affect the AMA,

whereas blocking of information from muscle spindle

receptors innervating the jaw-closing muscles abolished

the AMA preceding the tooth contact. Earlier animal

studies have shown that combined destruction of

periodontal receptors and muscle-spindle receptors

diminish the AMA almost completely, while destruc-

tion of either one of both receptors do not completely

diminish the AMA (34, 35, 42). These results suggest

that the timing of the predictive component of the

AMA may be controlled mainly by information from

muscle spindles, while the magnitude of the AMA is

under the control of both muscle spindles and perio-

dontal receptors (41). Furthermore, blocking of infor-

mation from periodontal receptors in anaesthetized

rabbits significantly reduces the build-up speed of the

masticatory force during chewing (43). Thus, informa-

tion acquired by periodontal receptors early after

contact during each chewing cycle may be used to

scale the muscle commands of the ensuing power phase

to the current food impedance. Indeed, jaw actions



observably adapt to the gradually changing mechanical

properties of a bolus also during natural chewing (34,

44–46). Interestingly, in contrast to subjects with their

natural teeth, patients with prostheses supported by

dental implants seem to chew with about the same

pattern of muscle activity throughout the entire mas-

ticatory sequence (47). The lack of adaptation in these

patients can be reasonably attributed to the absence of

periodontal receptors.

In summary, signals from periodontal receptors are

used in the fine motor control of jaw actions associated

with biting, intraoral manipulation and the chewing of

food. It is clear from studies of various patient groups

(e.g. patients with dental implants) that important

sensory-motor functions are lost or impaired when

these receptors are removed during the extraction of

teeth. This knowledge emphasizes the importance of

maintaining natural teeth with healthy periodontal

function whenever possible.

Acknowledgments

This work was supported by the Karolinska Institute

and the Swedish Medical Research Council.

References

1. Lund JP. Mastication and its control by the brain stem. Crit

Rev Oral Biol Med. 1991;2:33–64.

2. Trulsson M, Johansson RS. Encoding of tooth loads by human

periodontal afferents and their role in jaw motor control. Prog

Neurobiol. 1996;49:267–284.

3. Turker KS. Reflex control of human jaw muscles. Crit Rev

Oral Biol Med. 2002;13:85–104.

4. Hannam AG. The innervation of the periodontal ligament. In:

Berkovitz BKB, Moxham BJ, Newman HN, eds. The Perio-

dontal Ligament in Health and Disease. Oxford: Pergamon,

1982: pp. 173–196.

5. Linden RWA. Periodontal mechanoreceptors and their func-

tions. In: Taylor A ed. Neurophysiology of the Jaws and Teeth.

New York: Macmillan, p. 52–88.

6. Vallbo AB, Hagbarth KE. Activity from skin mechanoreceptors

recorded percutaneously in awake human subjects. Exp

Neurol. 1968;21:270–289.

7. Johansson RS, Olsson KA. Microelectrode recordings from

human oral mechanoreceptors. Brain Res. 1976;118:

307–311.

8. Trulsson M, Johansson RS, Olsson KA. Directional sensitivity

of human periodontal mechanoreceptive afferents to forces

applied to the teeth. J Physiol Lond. 1992;447:373–389.

9. Dong WK, Shiwaku T, Kawakami Y, Chudler EH. Static and

dynamic responses of periodontal ligament mechanoreceptors

and intradental mechanoreceptors. J Neurophysiol.

1993;69:1567–1582.

10. Johnsen SE, Trulsson M. Receptive field properties of human

periodontal afferents responding to loading of premolar and

molar teeth. J Neurophysiol. 2003;89:1478–1487.

11. Sakada S, Kamio E. Receptive fields and directional sensi-

tivity of single sensory units innervating the periodontal

ligament of the cat mandibular teeth. Bull Tokyo Dent Coll.

1971;12:25–43.

12. Karita K, Tabata T. Response fields of the periodontal

mechanosensitive units in the superior alveolar nerve of the

cat. Exp Neurol. 1985;90:558–565.

13. Hannam AG. Receptor fields of periodontal mechanosensitive

units in the dog. Arch Oral Biol. 1970;15:971–978.

14. Trulsson M. Multiple-tooth receptive fields of single human

periodontal mechanoreceptive afferents. J Neurophysiol.

1993;69:474–481.

15. Edin BB, Trulsson M. Neural network analysis of the infor-

mation content in population responses from human perio-

dontal receptors. Proc. SPIE. 1992;1710:257–266.

16. Johansson RS, Vallbo AB. Spatial properties of the population

of mechanoreceptive units in the glabrous skin of the human

hand. Brain Res. 1980;184:353–366.

17. Johnsen SE, Trulsson M. Encoding of amplitude and rate of

tooth loads by human periodontal afferents from premolar

and molar teeth. J Neurophysiol. 2005;93:1889–1897.

18. Passatore M, Lucchi ML, Filippi GM, Manni E, Bortolami R.

Localization of neurons innervating masticatory muscle spin-

dle and periodontal receptors in the mesencephalic trigeminal

nucleus and their reflex actions. Arch Ital Biol. 1983;121:117–

130.

19. Byers MR, Dong WK. Comparison of trigeminal receptor

location and structure in the periodontal ligament of different

types of teeth from the rat, cat, and monkey. J Comp Neurol.

1989;279:117–127.

20. Hassanali J. Quantitative and somatotopic mapping of neu-

rones in the trigeminal mesencephalic nucleus and ganglion

innervating teeth in monkey and baboon. Arch Oral Biol.

1997;42:673–682.

21. Johansson RS, Vallbo AB. Tactile sensory coding in the glabrous

skin of the human hand. Trends Neurosci. 1983;6:27–31.

22. Siebert G. Recent results concerning physiological tooth

movement and anterior guidance. J Oral Rehabil.

1981;8:479–493.

23. Miura H, Hasegawa S, Okada D, Ishihara H. The measurement

of physiological tooth displacement in function. J Med Dent

Sci. 1998;45:103–115.

24. Trulsson M, Johansson RS. Encoding of amplitude and rate of

forces applied to the teeth by human periodontal mechano-

receptive afferents. J Neurophysiol. 1994;72:1734–1744.

25. Pfaffmann C. Afferent impulses from the teeth due to pressure

and noxious stimulation. J Physiol. 1939;97:207–219.

26. Ness AR. The mechanoreceptors of the rabbit mandibular

incisor. J Physiol. 1954;126:475–493.

27. Hannam AG. The response of periodontal mechanoreceptors

in the dog to controlled loading of the teeth. Arch Oral Biol.

1969;14:781–791.



28. Hannam AG, Farnsworth TJ. Information transmission in

trigeminal mechanosensitive afferents from teeth in the cat.

Arch Oral Biol. 1977;22:181–186.

29. Trulsson M, Johansson RS. Forces applied by the incisors and

roles of periodontal afferents during food-holding and -biting

tasks. Exp Brain Res. 1996;107:486–496.

30. Trulsson M, Johansson RS. Human periodontal mechanore-

ceptors: encoding of force and role in control of jaw actions.

In: Morimoto T, Matsuya T, Takada K eds. Brain and Oral

Functions Oral Motor Function and Dysfunction. Amsterdam:

Elsevier Science, 1995:155–163.

31. De Boever JA, McCall WD Jr, Holden S, Ash MM Jr.

Functional occlusal forces: an investigation by telemetry.

J Prosthet Dent. 1978;40:326–333.

32. Appenteng K, Lund JP, Seguin JJ. Intraoral mechanoreceptor

activity during jaw movement in the anesthetized rabbit.

J Neurophysiol. 1982;48:27–37.

33. Trulsson M, Gunne HSJ. Food-holding and -biting behavior in

human subjects lacking periodontal receptors. J Dent Res.

1998;77:574–582.

34. Inoue T, Kato T, Masuda Y, Nakamura T, Kawamura Y,

Morimoto T. Modifications of masticatory behaviour after

trigeminal deafferentation in the rabbit. Exp Brain Res.

1989;74:579–591.

35. Lavigne G, Kim JS, Valiquette C, Lund JP. Evidence that

periodontal pressoreceptors provide positive feedback to jaw

closing muscles during mastication. J Neurophysiol.

1987;58:342–358.

36. Johansson RS, Westling G. Signals in tactile afferent from the

fingers eliciting adaptive motor responses during precision

grip. Exp Brain Res. 1987;66:141–154.

37. Westling G, Johansson RS. Responses in glabrous skin

mechanoreceptors during precision grip in humans. Exp Brain

Res. 1987;66:128–140.

38. Johansson RS. Dynamic use of tactile afferent signals in

control of dexterous manipulation. Adv Exp Med Biol.

2002;508:397–410.

39. Ottenhoff FA, van der Bildt A, van der Glas HW, Bosman F.

Peripherally induced and anticipating elevator muscle activity

during simulated chewing in humans. J Neurophysiol.

1992;67:75–83.

40. Ottenhoff FA, van der Bildt A, van der Glas HW, Bosman F.

Control of elevator muscle activity during simulated chewing

with varying food resistance in humans. J Neurophysiol.

1992;68:933–944.

41. Komuro A, Morimoto T, Iwata K, Inoue T, Masuda Y, Kato T,

Hidaka O. Putative feed-forward control of jaw-closing muscle

activity during rhythmic jaw movements in the anesthetized

rabbit. J Neurophysiol. 2001;86:2834–2844.

42. Morimoto T, Inoue T, Masuda Y, Nagashima T. Sensory

components facilitating jaw-closing muscle activities in the

rabbit. Exp Brain Res. 1989;76:424–440.

43. Hidaka O, Morimoto T, Masuda Y, Kato T, Matsuo R, Inoue T,

Kobayashi M, Takada K. Regulation of masticatory force

during cortically induced rhythmic jaw movements in the

anesthetized rabbit. J Neurophysiol. 1997;77:3168–3179.

44. Thexton AJ, Hiiemae KM, Crompton AW. Food consistency

and bite size as regulators of jaw movement during feeding in

the cat. J Neurophysiol. 1980;44:456–474.

45. Plesh O, Bishop B, McCall W. Effect of gum hardness on

chewing pattern. Exp Neurol. 1986;92:502–512.

46. Schwartz G, Enomoto S, Valiquette C, Lund JP. Mastication in

the rabbit: a description of movement and muscle activity.

J Neurophysiol. 1989;62:273–287.

47. Haraldson T. Comparisons of chewing patterns in patients

with bridges supported on osseointegrated implants and

subjects with natural dentitions. Acta Odontol Scand.

1983;41:203–208.

Correspondence: Dr M. Trulsson, Institute of Odontology, Karolinska

Institutet, Box 4064, S-141 04 Huddinge, Sweden.

E-mail: [email protected]



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