Temporal profile and amplitude of human masseter muscle activity is adapted to food properties during individual chewing cycles

Abstract

Jaw actions adapt to the changing properties of food that occur during a masticatory sequence. In the present study, we investigated how the time-varying activation profile of the masseter muscle changes during natural chewing in humans and how food hardness affects the profile. We recorded surface electromyography (EMG) of the masseter muscle together with the movement of the lower jaw in 14 healthy young adults (mean age 22) when chewing gelatin-based model food of two different hardness. The muscle activity and the jaw kinematics were analysed for different phases of the chewing cycles. The increase in the excitatory drive of the masseter muscle was biphasic during the jaw-closing phase showing early and late components. The transition between these components occurred approximately at the time of tooth–food contact. During the masticatory sequence, when the food was particularised, the size of the early component as well as the peak amplitude of the EMG significantly decreased along with a reduction in the duration of the jaw-closing phase. Except for amplitude scaling, food hardness did not appreciably affect the muscle's activation profile. In conclusion, when chewing food during natural conditions, masseter muscle activation adapted throughout the masticatory sequence, principally during the jaw-closing phase and influenced both early and late muscle activation components. Furthermore, the adaptation of jaw actions to food hardness was affected by amplitude scaling of the magnitude of the muscle activity throughout the masticatory sequence.

Full text

Temporal profile and amplitude of human masseter muscle
activity is adapted to food properties during individual
chewing cycles
A. GRIGORIADIS*, R. S. JOHANSSON
†
& M. TRULSSON* *Department of Dental Medicine,
Karolinska Institutet, Huddinge, and
†
Department of Integrative Medical Biology, Ume

a University, Ume

a, Sweden
SUMMARY Jaw actions adapt to the changing
properties of food that occur during a masticatory
sequence. In the present study, we investigated how
the time-varying activation profile of the masseter
muscle changes during natural chewing in humans
and how food hardness affects the profile. We
recorded surface electromyography (EMG) of the
masseter muscle together with the movement of
the lower jaw in 14 healthy young adults (mean age
22) when chewing gelatin-based model food of two
different hardness. The muscle activity and the jaw
kinematics were analysed for different phases of the
chewing cycles. The increase in the excitatory drive
of the masseter muscle was biphasic during the jaw-
closing phase showing early and late components.
The transition between these components occurred
approximately at the time of tooth–food contact.
During the masticatory sequence, when the food
was particularised, the size of the early component
as well as the peak amplitude of the EMG
significantly decreased along with a reduction in the
duration of the jaw-closing phase. Except for
amplitude scaling, food hardness did not
appreciably affect the muscle’s activation profile. In
conclusion, when chewing food during natural
conditions, masseter muscle activation adapted
throughout the masticatory sequence, principally
during the jaw-closing phase and influenced both
early and late muscle activation components.
Furthermore, the adaptation of jaw actions to food
hardness was affected by amplitude scaling of the
magnitude of the muscle activity throughout the
masticatory sequence.
KEYWORDS: electromyography, food, kinematics,
masseter muscle, mastication, neurophysiology
Accepted for publication 6 February 2014
Background
During mastication, rhythmical jaw movements break
down the food to a bolus that can be easily swal-
lowed. A central pattern generator located in the
brain stem accounts for the basic rhythm and coordi-
nation of jaw muscle commands during mastication
(1, 2). However, the final output to the jaw muscles
is modulated by various factors, including sensory
inputs signalling the properties of the food (3, 4). In
human studies, while chewing on elastic model food
with controlled hardness, it has been observed that
the muscle activity adapt to food hardness and the
changing properties of the food that occur during a
masticatory sequence (5–7). Although, several differ-
ent types of mechanoreceptors in oro-facial tissues
contribute to this sensorimotor regulation (8), the
muscle spindles in the jaw-closing muscles and the
periodontal mechanoreceptors are considered prime
contributors (9–11).
Studies in humans performing simulated chewing
movements indicated that a fraction of the observed
muscle activity was needed to move the jaw, whereas
most of the activity referred as ‘additional muscle
©2014 John Wiley & Sons Ltd doi: 10.1111/joor.12155
Journal of Oral Rehabilitation 2014
Journal o f Oral Rehabilitation

activity (AMA)’, was used to overcome the resistance
of food (12, 13). These studies also suggested that the
nervous system uses two parallel strategies to regu-
late AMA. A feed-forward strategy contributes to
scale the intensity of the muscle commands based on
prediction of food resistance, and a feedback process
was used to adjust muscle activity based on informa-
tion about the mechanical properties of the food
obtained from periodontal mechanoreceptors and
muscle spindles in jaw-closing muscles. While akin
control strategies have been observed in experiments
on anaesthetised rabbits during cortically induced
chewing (14, 15), they have not been demonstrated
in humans during natural chewing. The present
study addresses, for the first time, these issues during
natural chewing in humans by examining the time-
varying activation profile of the masseter muscle dur-
ing individual chewing cycles and its changes during
masticatory sequences carried out with food of differ-
ent hardness.
Materials and methods
Participants
The study included 14 healthy participants (nine
females) with natural dentition and at least 28 perma-
nent teeth (age range 22–26 years). None of the par-
ticipants had any known dental pathology and none
indicated problems or dysfunctions with eating.
Recording equipment and experimental protocol
Apparatus and general experimental procedures have
previously been described (5). Briefly, seated partici-
pants chewed and swallowed three soft and three hard
visco-elastic model types of food while we recorded
the three-dimensional movements of the lower jaw
(Fig. 1a). The jaw movement was measured with a
frame attached to the head and equipped with an array
of magnetic sensors (accuracy: 01 mm; bandwidth:
DC –100 Hz) that tracked a magnet (10 9595 mm)
that was attached on the mandibular incisors. The food
samples were based on gelatin of two different grades
(one for soft and one for hard food) and had a cylindri-
cal shape (diameter: 20 mm; height: 10 mm). We per-
formed duplicate measurements of the mechanical
properties of samples from each batch of model food
using a compressing machine (Autograph control/mea-
suring unit*) to verify the visco-elastic properties. The
order of food presentation, hard or soft samples was
unpredictable and counter-balanced across the partici-
pants. Surface EMG-signals were recorded from the
centre of the masseter muscle located on the preferred
chewing side, which was determined before the exper-
iment by asking participants which side they preferred
to chew if they had to make a choice. Bipolar surface
electrodes (2 mm in diameter and 12 mm apart) were
used. Shielded differential pre-amplifiers (bandwidth
6Hz–25 kHz) were located on the skin directly above
the integrated surface electrodes. All signals recorded
were stored and analysed using the SC/ZOOM micro-
computer-based data acquisition and analysis system
(SC/ZOOM, v.3.1.02, Ume

a University, Physiology
Section
†
). The EMG signals were sampled at 32 kHz,
and the vertical position of the lower jaw was sampled
at 800 Hz.
Data analysis
Analysis was focused on three segments of each mas-
ticatory sequence that represented its beginning, mid-
dle and end, and each segment was represented by
three consecutive cycles across which data were aver-
aged (5) (Fig. 1b). We defined a chewing cycle, con-
sisting of an opening phase followed by a closing
phase and occlusal phase (Fig. 1c). In addition, for
each chewing cycle, we measured the duration of
each of the three phases together with the peak verti-
cal amplitude and peak closing velocity of the jaw
movements during chewing. To make EMG data
comparable across participants, we normalised the
time-varying EMG signal by dividing it by the mean
activity averaged across all chewing cycles for each
participant (5). To preserve temporal phase informa-
tion during averaging of the time varying data across
chewing cycles, for each cycle we normalised the time
base by scaling each phase to the mean duration of
that phase computed across all relevant cycles for all
participants (Fig. 1d). The transition between the
early and late component was empirically defined as
the first point after the start of the jaw-closing phase
where the second derivate of the EMG signal reached
300 normalised units s
2
(NU s
2
).
*AG-G Shimadzu, Kyoto, Japan.
†
IMB, Ume

a, Sweden.
©2014 John Wiley & Sons Ltd
A. GRIGORIADIS et al.
2

Point estimates of jaw movement and EMG data
averaged within subjects were subjected to repeated
measures ANOVAs with segment of the masticatory
sequence (beginning, middle and end) and type of
food (hard and soft) as fixed effects. A P-value <005
was considered statistically significant.
Results
In agreement with previous findings, the participants
used a larger number of chewing cycles with hard food
(270139) than with soft food (21095;
mean SD, N=14) and longer sequence durations
with harder food (21374 s) compared to soft food
(16466 s) (3, 5, 7). Furthermore, the vertical
amplitude of jaw movement was greater with the hard
food than with soft (F
1:13
=3424; P<0001; Fig. 2a),
and it decreased during the progression of the mastica-
tory sequence (F
2:26
=266; P<0001; Fig. 2a).
Duration of chewing cycles was not appreciably
affected by the type of food (hard, soft) and their
position in the masticatory sequence (beginning, mid-
dle and end). However, duration of the various phases
of the chewing cycles (opening, closing and occlusal
Masseter EMG
Vertical position
0·5 mV
10 mm
5 s
(b)
One cycle
(a)
BM
x
z
y
Vertical
position
Masseter
EMG
E
Opening
Closing
Occlusal
(c)
Magnetic
sensors
EMG
electrode
Permanent
magnet
Masseter
EMG (NU)
0
1
2
3
Vertical
position (mm)
0
5
10
15
Single chewing
cycles
Normalized cycles
averaged
0 200–200–400
Single cycles,
time normalized
0 200–200–400 0 200–200–400
Time (ms)
(d)
Fig. 1. Jaw movements and muscular activity during chewing of model foods. (a) Electromyographic (EMG) activity recorded from
the centre of the masseter muscle using bipolar surface electrodes (2 mm in diameter and 12 mm apart; bandwidth 6 Hz–25 kHz).
Jaw movements were recorded by means of a small permanent magnet attached to the labial surfaces of the lower incisors, whose
position was tracked with magnetic sensors attached to the head via a lightweight head mounted frame (accuracy: 01 mm; band-
width: DC –100 Hz). (b) Vertical position of the mandible and EMG activity (root-mean-square processed) during an exemplar masti-
catory sequence. Grey boxes indicate segments of the masticatory sequence representing its beginning (B), middle (M) and end
(E). (c) Close-up of the middle segment with the opening, closing and occlusal phase demarcated for the central chewing cycle. Jaw-
opening phase began when the jaw was opened from the occlusal state by 1 mm and ended at peak jaw opening and was followed by
the closing phase that ended when the jaw reached the same vertical position as where the opening phase began. The occlusal phase
started at the end of the closing phase and ended at the beginning of the opening phase of the subsequent chewing cycle. (d) Time
normalisation of nine chewing cycles (3 cycles 93 sequences) collected at the beginning of the masticatory sequence from one partic-
ipant chewing hard food. The recorded cycles, aligned at the onset of the occlusion phase (left panel), were normalised to the mean
duration of each of the phases (middle panel) and averaged (right panel; mean SE).
©2014 John Wiley & Sons Ltd
TEMPORAL PROFILE OF HUMAN MASSETER MUSCLE ACTIVITY 3

phases) changed during the masticatory sequence
(Fig. 2b). The duration of opening and closing phases
decreased (F
2:26
=54; P=001 and F
2:26
=187;
P<0001), whereas duration of the occlusal phase
increased (F
2:26
=92; P<0001). Food hardness had
no main effect on the duration of any of the phases
but food and segment interacted on the duration of
the opening phase (F
2:26
=55; P=001). In essence,
only hard food changed the duration of the opening
phase during the masticatory sequence. Interestingly,
the period during which jaw-closing muscles were
active, corresponded to the duration of the closing
and the occlusal phases together (see further below).
Neither were significantly affected by food
(F
1:13
=30; P=011) nor the position of the chewing
cycle in the masticatory sequence (F
2:26
=09;
P=042).
Figure 3a illustrates changes during the masticatory
sequence in vertical jaw movements and masseter
EMG when participants chewed hard food. As the food
was particularised, the masseter EMG activity inte-
grated over the whole chewing cycle gradually
decreased during the masticatory sequence
(F
2:26
=409; P<0001). Similarly, the peak EMG was
also reduced during the masticatory sequence
(F
2:26
=38; P<005). Moreover, the time of peak
EMG activity, with reference to the onset of the occlu-
sal phase, gradually shifted during the sequence
(F
2:26
=52; P<005). In its beginning and middle, the
peak preceded the onset of the occlusal phase on aver-
age by 159132 ms and 13867 ms, respec-
tively, whereas at the end it lagged the onset by
20365 ms (mean SEM, N=14). Accordingly,
EMG activity integrated over the jaw-closing phase
gradually decreased during the sequence (F
2:26
=756;
P<0001), whereas the activity integrated over the
occlusal phase did not significantly change (F
2:26
=099;
P=039).
The temporal profile of EMG activity during the
jaw-closing phase suggested that the increase in the
excitatory drive of masseter muscle was biphasic,
showing an early and a later component. Figure 3b
highlights the biphasic nature of the muscle drive by
showing the first time differential of the EMG signals
shown in Fig. 3a.
Interestingly, during the first segment of the masti-
catory sequence, the estimated transition between the
early and late component (see arrowheads in Fig. 3a,
b) occurred when the jaw opened around 11 mm,
corresponding to the size of the model food. This sug-
gests that the transition occurred around the time of
food contact. In accordance with a gradual reduction
in the size of the food particles, the transition
occurred at smaller jaw openings in subsequent seg-
ments (F
2:26
=423; P<0001; Fig. 3c).
As can be seen in Fig. 3b, the rate of increase for
the early EMG component gradually declined during
the masticatory sequence (F
2:26
=539; P<0001).
The peak was 10624, 5619 and 2812
NU s
1
in the beginning, middle and end, respec-
tively, suggesting that muscle activity, reflected by the
early EMG component, accelerated the mandible
BME
10
15
20
Amplitude of vertical
jaw movement (mm)
Hard food
Soft food
(a)
0·2 0·2 0·2
0·3 0·3 0·3
0·4 0·4 0·4
BBB
Segment of masticatory sequence
MMMEEE
Opening Occlusal
Phase duration (s)
Hard food
Soft food
Closing
SEM
SD
(b)
SEM
SD
Fig. 2. Jaw movement variables during the masticatory sequences. (a) Vertical amplitude during the three segments (beginning,
middle and end) of the masticatory sequence when chewing hard and soft food. (b) Duration of opening, closing and occlusal phases
of chewing cycles at the beginning, middle and end of the masticatory sequence performed with hard and soft food. Data averaged
across all participants. Vertical bars indicate unilaterally 1 s.d. and 1 s.e.m. (N=14).
©2014 John Wiley & Sons Ltd
A. GRIGORIADIS et al.
4

before food contact. Indeed, peak jaw-closing velocity
was highest at the beginning and gradually declined
during the masticatory sequence (F
2:26
=80;
P<001).
Figure 4 illustrates the effect of food hardness on the
temporal activation profile of the masseter muscle.
Both food type and segment of the masticatory
sequence had their main effects on peak amplitude of
the masseter EMG (F
1:13
=502; P<0001 and
F
2:26
=35; P<005, respectively). Chewing soft food
was associated with lower peak amplitude of the mas-
seter EMG compared to chewing hard food, and as
addressed above, the activity declined during the
masticatory sequence. Overall, our results suggest a
proportional scaling of EMG amplitude to food type
during the masticatory sequence. This was verified by
an interaction between food and segment that
approached significance (F
2:26
=32; P=0059) and
that the temporal profile was similar for hard and soft
food throughout the masticatory sequence (see inset in
Fig. 4a–c). Furthermore, food hardness did not affect
time of peak of EMG activity with reference to the
onset of the occlusal phase in any segment of the mas-
ticatory sequence (P>005 in each case). Finally, an
early and a late component of EMG increase during the
jaw-closing phase could be discerned with soft food
also.
Discussion
In agreement with previous studies, we found that
the activity in jaw-closing muscles adapted to food
hardness and to changing properties of the food
during a masticatory sequence (5–7). One central
finding in this study was that the temporal profile of
muscle activity was virtually identical when humans
naturally chewed hard and soft food, implying that
the principal effect of food hardness was due to scal-
ing in the magnitude of activity. A second advance
was the demonstration that during natural chewing
(a)
Rate of change of EMG activity
(b)
Beginning
End
Middle
100 ms
(c)
Beginning Middle End
8
10
12
14
16
Vertical amplitude (mm)
SEM
SD
Vertical amplitude (mm)
Time (ms)
0
5
10
15
Beginning
End
Middle
BME
BME
EMG activity (NU)
1
Beginning
Middle
End
–400 –200–600 200
0
Fig. 3. Vertical jaw movements and masseter electromyography (EMG) calibrated in normalised units (NU) during single chewing
cycles when participants chewed hard food. (a) Data was averaged across all participants and chewing cycles in the beginning, middle
and end segment of the masticatory sequence after the time base had been normalised by scaling each phase of each chewing cycle to
the mean duration of that phase across all participants. Data temporally aligned at the start of the occlusal phase (dashed vertical line
at time =0) and curves give mean values and grey zones indicate s.e. (N=14). The vertical lines to the left and right show the
time of peak jaw opening indicating the start of the closing phase and the end of the occlusal phase respectively, for data representing
the beginning, middle and the end of the masticatory sequence. Arrowheads indicate the transition from the early to the late compo-
nents of the increase of EMG activity during the closing phase. (b) Rate of change as a function of time of the averaged EMG signals
shown in (a). Arrowheads indicates the transition between the early to late EMG components. (c) Vertical amplitude of the mandible
movement at the transition-point between the early and late EMG components during the beginning, middle and end of the mastica-
tory sequence. Symbols indicate mean values across all participants and bars unilaterally 1 SD and 1 SEM (N=14).
©2014 John Wiley & Sons Ltd
TEMPORAL PROFILE OF HUMAN MASSETER MUSCLE ACTIVITY 5

the muscle drive in the jaw-closing phase had an
early and a late component. The early component,
which started just before the jaw-closing phase,
appeared to drive the mandible up to the point when
the teeth of the upper jaw were brought in contact
with the food and bite forces were generated. The
initiation of this early muscle activity would thus
determine the start of the jaw-closing phase. Presum-
ably, knowledge about the current properties of the
food, such as particle sizes and rheological properties,
acquired during previous chewing cycles was used to
adapt predictively this muscle activity during the mas-
ticatory sequence. Indeed, the start of the jaw-closing
phase occurred at gradually smaller jaw openings dur-
ing the progression of the masticatory sequence and
the food were gradually more particularised. Likewise,
the rate of increase in muscle activation during the
early component declined during the masticatory
sequence, which matched the gradually smaller accel-
eration of the mandible during jaw closing.
A third central finding in this study was that the
decrease in jaw muscle activity during the masticatory
sequence occurred essentially during the jaw-closing
phase and involved adaptation of both early and late
components. During the masticatory sequence, the
duration of the jaw-closing phase decreased. At the
same time, the rate of EMG increase of the early com-
ponent and the peak EMG of the late component
decreased.
The transition between the early and the late com-
ponent of muscle activation during the jaw-closing
phase appeared to occur around the time that the
teeth began to apply forces onto the food. Given their
high sensitivity at low contact forces (9, 16, 17), sig-
nals from periodontal mechanoreceptors could have
contributed to the initiation of the late component.
Regarding its regulation, studies in humans perform-
ing simulated chewing movements suggest that two
parallel control strategies regulate muscle activity gen-
erated to overcome the resistance of food during
chewing (12, 13): The underlying muscle commands
were partly parameterised in advance using prediction
of food resistance based on sensory experiences dur-
ing preceding chewing cycles and partly modulated
online by direct feedback information from oral me-
chanoreceptors. Regarding the latter, animal studies
have suggested that signals from muscle spindles were
most important during the early phases of force gen-
eration, whereas inputs from both muscle spindles
and periodontal mechanoreceptors were important for
the later part (14, 15, 18–20).
Taken together, predictions of food properties based
on information obtained during previous chewing
cycles plays an essential role in regulating, in a
parametric manner, both the early and the late
components of jaw muscle activation during the
Vertical amplitude (mm)
0
5
10
15
Vertical amplitude (mm)
0
5
10
Vertical amplitude (mm)
0
5
10
15
0–200
–400–600 200
Time (ms)
(a)
Hard food
Soft food
Hard food
Soft food
Beginning
Middle
End
Soft food
Hard food
Hard food
Soft food
Hard food
Soft food
Soft food
Hard food
Soft food
Hard food
Hard food
Soft food
Hard food
Soft food
EMG (NU)
1
EMG (NU)
1
EMG (NU)
1
(b)
(c)
Fig. 4. Vertical jaw position and masseter EMG activity when
chewing hard (solid curves) and soft food (dashed curves). (a–c)
refers to the beginning, middle and end of the masticatory
sequence. Format and details as in Fig. 3a. The inset in the
lower left corner of each panel illustrates the mean muscle
activity for hard and soft foods after normalisation to peak
amplitude. EMG, electromyography.
©2014 John Wiley & Sons Ltd
A. GRIGORIADIS et al.
6

jaw-closing phase to the changing mechanical proper-
ties of the food during natural mastication. Since peri-
odontal afferents are particularly suited to convey
detailed information about the contact state between
food and dentition during biting and chewing (9, 16,
17, 21, 22), these afferents presumably play a pivotal
role in providing information about the mechanical
properties of food used for control of subsequent
mandibular actions. Indeed, people with implant-sup-
ported bridges, who lack periodontal mechanorecep-
tors, show an impaired capacity to adapt chewing
behaviour to food hardness (5).
Acknowledgments
The study was approved by the local ethical commit-
tee. This work was funded by the Strategic Research
Program in Neuroscience at the Karolinska Institutet,
the Swedish Dental Society, King Gustaf V’s and
Queen Victoria’s Freemason Foundation, American
Dental Society of Sweden and Stockholm County
Council. The authors declare that they have no con-
flict of interests. We thank A. B€
ackstr€
om, G. Westling
and M.

Aberg for their technical support.
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Correspondence: Anastasios Grigoriadis, Department of Dental
Medicine, Karolinska Institutet, PO Box 4064, SE-141 04 Huddinge,
Sweden. Email: anastasios.grigoriadis@ki.se
©2014 John Wiley & Sons Ltd
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