RECONSTRUCTIVE
A Functional Magnetic Resonance Imaging
Paradigm to Identify Distinct Cortical Areas ofFacial Function: A Reliable Localizer
Marco Romeo, M.D.
Luca Vizioli, Ph.D.
Myrte Breukink, M.D.
Kiomars Aganloo, M.D.
Junpeng Lao
Stefano Cotrufo, Ph.D.
Roberto Caldara, Ph.D.
Stephen Morley, F.R.C.S.Plast.
Fribourg, Switzerland;
Glasgow, United Kingdom; andGroningen, The Netherlands

Background: Irreversible facial paralysis can be surgically treated by importing
both a new neural and a new motor muscle supply. Various donor nerves can beused. If a nerve supply other than the facial nerve is used, the patient has to adapt
to generate a smile. If branches of the fifth cranial nerve are used, the patient has
to learn to clench teeth and smile. Currently, controversy exists regarding whether
a patient develops a spontaneous smile if a nerve other than the facial nerve is used.
The authors postulate that brain adaptation in facial palsy patients can occur
because of neural plasticity. The authors aimed to determine whether functional
magnetic resonance imaging could topographically differentiate activity between
the facial nerve– and the trigeminal nerve–related cortical areas.
Methods: A new paradigm of study using functional magnetic resonanceimaging based on blood oxygen level– dependent signal activation was tested
on 15 voluntary healthy subjects to find a sensitive localizer for teeth clenching and smiling. Subjects smiled to stimulate the facial nerve–related cortex,
clenched their jaws to stimulate the trigeminal nerve–related cortex, andtapped their finger as a control condition.
Results: Smiling and teeth clenching showed distinct and consistent areas ofcortical activation. Trigeminal and facial motor cortex areas were found to be
distinct areas with minimal overlapping.
Conclusions: The authors successfully devised a functional magnetic resonanceimaging paradigm effective for activating specific areas corresponding to teeth
clenching and smiling. This will allow accurate mapping of cortical plasticity infacial reanimation patients. (Plast. Reconstr. Surg. 131: 527e, 2013.)
CLINICAL QUESTION/LEVEL OF EVIDENCE: Diagnostic, IV.

F

acial reanimation surgery following irreversible facial paralysis can be achieved with several
surgical procedures. Generally speaking, botha strengthened or new nerve supply and a new muscle supply are required to recreate the smile. If thecontralateral facial nerve is used as a donor nerve, itis generally accepted that a spontaneous, emotionFrom the Department of Psychology, University of Fribourg;
the Center for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow; the Canniesburn Plastic Surgery Unit, Glasgow Royal Infirmary; andUniversity Medical Center Groningen.
Received for publication July 26, 2012; accepted November
1, 2012.
Presented at the 23rd Annual Meeting of the European
Association of Plastic Surgeons, in Munich, Germany, May
24 through 26, 2012, and the 15th Annual Meeting of theEuropean Conference of Scientists and Plastic Surgeons, inPamplona, Spain, October 28 through 29, 2011.
Copyright ©2013 by the American Society of Plastic Surgeons
DOI: 10.1097/PRS.0b013e3182818b68

ally driven smile can be achieved. If another nerve,
most commonly the trigeminal, is used, however,significant controversy exists as to whether a spontaneous smile can ever be achieved.
The facial nerve is a complex motor/sensitive
structure, partially crossed, giving fine movement toa high number of muscles. The choice of surgicalreanimation technique is determined mainly by thecause of facial paralysis and by the age and desires ofthe patient. The techniques most commonly used
are the nerve grafts (sixth to seventh, twelfth toseventh, and cross-facial nerve graft),1,2 dynamic
muscle transfers (temporal myoplasty, free muscle
transfer),3–9 and static suspension.10,11 Some procedures require a two-stage and some a one-stage
approach.

Disclosure: The authors have no potential financial interests to declare.

www.PRSJournal.com

527ePlastic and Reconstructive Surgery • April 2013
There remains substantial controversy as towhether it is important to use the facial nerve as anerve supply in facial reanimation or whether analternative nerve can lead to equivalent results. Using the facial nerve may require a two-stage procedure, especially if a muscle flap is needed. The advantage of using the facial nerve is that the resultant
smile will be spontaneous and emotional. In contrast, using a branch of the trigeminal nerve as the
motor source (such as the nerve to masseter) alongwith a free muscle transfer or a temporalis myoplasty
simplifies surgery, and results can be achieved in one
stage. However, it is still unclear whether using thetrigeminal nerve as a motor can lead to a natural,
spontaneous smile. At least initially, patients need tolearn to clench their teeth to initiate a “smile.” It couldbe, however, that, in time, the smile can become spontaneous, as a consequence of cerebral reorganization.
After central or peripheral injury, molecular
and/or structural alterations, also known as brain
plasticity,12–14 lead to a certain degree of functional
adaptation. This phenomenon is thought to beparticularly important in facial reanimation,
where a motor nerve other than the facial nerve isused to create a smile. We have hypothesized thatthese changes may be mapped using functional
magnetic resonance imaging. If this is the case, it
could be possible to objectively assess brain plasticity following facial reanimation surgery.
Functional magnetic resonance imaging has become the most useful tool with which to relate functional activity to specific anatomical locations in thebrain. In contrast to structural magnetic resonanceimaging, functional magnetic resonance imaging
detects changes in blood oxygenation (i.e., blood
oxygen level– dependent signal)15,16 because of small
distortions in the magnetic field as a consequence ofunbound iron to oxygen deoxyhemoglobin. Given
that whenever a part of the brain becomes active
oxygenated blood flow increases, blood oxygen level–
dependent signal changes can be related directly tobrain activation.
High spatial resolution of magnetic resonanceimaging coupled with blood oxygen level– dependent signal changes make quantitative and qualitative cortical activity imaging possible.17 Functional magnetic resonance imaging findings on
brain plasticity illustrate augmentation of bloodflow on the contralateral side18 and self-tuning of
inhibition or stimulation signals of the motor
cortex19,20 with expansion of the cortical representation near the injured area. Brain reorganization
occurs throughout life during learning processes,
novel experiences, and in response to injury12,21,22
or even after surgery.13

528eThis study aimed to localize cortical activation
during smiling (seventh cranial nerve), teeth clenching (fifth cranial nerve), and finger tapping (control) by using a specific functional magnetic resonance imaging paradigm to determine whether the
spatial resolution provided by functional magnetic
resonance imaging is accurate enough to consistently and reliably distinguish areas of cortical activation between smiling and teeth clenching.
These areas of the brain should correlate withactivity relating to smile using the facial nerve(represented as smiling in the paradigm) andbrain activity relating to a smile created using thetrigeminal nerve (represented as teeth clenchingin the paradigm). An effective protocol to measure brain plasticity could provide better understanding of the consequences and effectiveness ofvarious surgical procedures in facial reanimation.
By comparing groups of patients undergoing different surgical procedures, we will be able to measure any variation in brain plasticity. In turn, thisshould help clarify the controversy that exists as towhether reanimation techniques using a trigeminal donor (either nerve to masseter or temporalistransfer) truly can lead to a spontaneous smile
without conscious teeth clenching. We therefore
devised a paradigm to measure cortical activity inhealthy subjects while stimulating smiling andteeth clenching, to mimic activity of both the trigeminal and facial nerves, such as would occur insubjects after facial reanimation surgery using either the facial or trigeminal nerve motor nerve
supply.

PATIENTS AND METHODS

Fifteen participants (mean ⫾ SD age, 31 ⫾ 12.5
years; eight male and 14 right-handed participants)
with normal or corrected-to-normal vision were included in the study. All participants provided written
informed consent in accordance with proceduresand protocols approved by the local ethics committee of the Centre for Cognitive Neuroimaging, Department of Psychology of the University of Glasgow
and NHS Ethical Committee.
Design and Motor Tasks
In a block design, participants were required
to perform three motor tasks: smiling, jaw clenching, and finger tapping. Before the beginning of
the experiment, all subjects practiced each task
for approximately 15 minutes under the experimenter’s supervision. The smiling action consistedof a voluntary smile characterized by contraction of
the zygomatic major only, movement marked as Ac-

Volume 131, Number 4 • Identifying Areas of Facial Function
tion Unit 12 in the Facial Action Coding System.23
Teeth clenching was performed by asking for simple mandible elevation, whereas for finger tapping, participants used their thumb to tap theremaining fingertips.
In the scanner, participants were instructed toperform the motor tasks on visual cue (i.e., the wordcorresponding to the task of interest). Subjects
viewed the screen through binocular visual display
goggles (Nordic NeuroLab, Milwaukee, Wis.). The
experiment consisted of three 6-minute runs, interleaved with a T1-weighted high-resolution anatomical scan. Each run began with a white central fixation cross for 8000 msec, followed by a word cue(smile, clench, or tap) presented for 1800 msec, indicating the required motor response. A blinking central
fixation was then flashed for 500 msec (16 times), dictating the tempo of muscle contraction. Another fixation was subsequently presented for 11,200 msec, preceding the onset of the next cue. Each task was
repeated four times per run, with movement sequences lasting approximately 16 seconds. Trial order
was randomized, and eye fixation was centrally locked
throughout runs; participants were asked to minimize
other movements while performing the task.
Magnetic Resonance Imaging Data Acquisition
Magnetic resonance imaging data were collected with a 3-T Siemens Tim Trio System (Siemens Medical, Munich, Germany) with a 12-channel head coil and integrated parallel imaging
techniques (integrated parallel acquisition technique factor, 2). Blood oxygen level– dependent
signals were measured with an echo-planar imaging sequence (echo time, 30 msec, repetition time,2000 msec; field of view, 210 mm; flip angle, 62
degrees; 10 percent gap; 36 axial slices; voxel size,3 ⫻ 3 ⫻ 3 mm). The slices were positioned to cover
the whole brain. A high-resolution three-dimensional anatomical scan (three-dimensional magnetization prepared rapid gradient echo, 1 ⫻ 1 ⫻1-mm resolution) was obtained during the samesession as the functional scans.
Magnetic Resonance Imaging Data Processing
We used BrainVoyager QX software (Brain Innovation, Maastricht, The Netherlands) to analyze
blood oxygen level– dependent imaging data.
Functional images were preprocessed as follows:
first, a slice scan time correction was performed
using a sync interpolation algorithm. We then carried out offline three-dimensional motion correction using a trilinear interpolation algorithm: allvolumes were spatially aligned to the first volume

by rigid body transformations, and the roto-translation information was saved for subsequent elaborations. Spatial smoothing was subsequently implemented using a Gaussian kernel of 4 mm at full
width at half maximum. Temporal data were thus
filtered using voxelwise linear detrend and highpass filter at 0.01 Hz. The participant’s slice-based
functional scan was finally coregistered on theirthree-dimensional high-resolution structural scanand transformed into Talairach space.24
To identify the brain regions responding todifferent motor movement, we computed a general linear model with separate predictors for smiling, clenching, and tapping. Beta weights were
calculated and used in the contrast. Three regionsof interest were identified independently per participant in both hemispheres by means of linear
contrasts. There were two regions of interest—
smiling (smiling versus clenching and tapping)and clenching (clenching versus smiling and tapping)—and a control [tapping (tapping versus
smile and clenching)]. For all contrasts, a t map
with a maximum threshold of p ⬍ 0.01 (false discovery rate corrected) was applied. Cluster sizes ofgreater than 0.27 cm3 (⬎10 voxels; voxel size after
normalization, 3 ⫻ 3 ⫻ 3 mm) showing a statistically significant Z score (typically, Z threshold ⫽3.0) in the comparison were considered.

RESULTS
Comparison between the motor tasks demonstrated no overlap between smiling and teeth
clenching regions of interest. The smiling task wassignificantly associated with increased blood oxygen level– dependent activation in intensive bilateral regions of the primary motor cortex, within
the middle precentral gyrus for all of the participants(p ⬍ 0.01, false discovery rate corrected, 10 voxels
minimum) (Table 1 and Figs. 1 and 2). By contrast,
a significantly larger activation for clenching compared with smiling plus tapping was identified ina distinct region in the low precentral gyrus of
most participants (n ⫽ 13 of 15 in the left hemisphere, n ⫽ 13 of 15 in the right hemisphere)(Table 1 and Fig. 2). As shown in Figure 1, thegroup coordinates for the smile region were 47,⫺12, 37 (right, Z ⫽ 18.291, size ⫽ 277 voxels) and⫺50, ⫺14, 36 (left, Z ⫽ 18.113, size ⫽ 302 voxels).
Accordingly, the group coordinates for the
clenching region were 54, ⫺8, 27 (right, z ⫽11.321, size ⫽ 254 voxels) and ⫺60, ⫺8, 31 (left,
Z ⫽ 10.913, size ⫽ 66 voxels).
Three participants also showed significantly
larger activation for smiling compared with clenching and tapping in the bottom region of the right

529e

530e
37.76 ⫾ 2.93

z
35.53
48.19
29.47
28.75
23.64
24.44
28.02
29.98
21.22
24.17
37.81
34.06
26.18
15.14
29.04 ⫾ 8.08

⫺7.31
⫺11.14
⫺7.32
0.5
⫺5.19
⫺8.15
⫺8.91
⫺5.91
⫺15.55⫺6.53⫺5.07⫺12.44⫺5.89⫺18.38⫺8.38 ⫾ 4.75

54.33
54.28
46.44
61.32
52.15
55.64
48.57
57.36
45.21
57.32
57

55.79
57.98
57.59
54.36 ⫾ 4.68

9.084
6.521
9.287
7.863
8.33
9.431
9.466
8.105
6.882
8.146
13.829
5.334
5.018
5.018
4.534
8.512
6.721
10.796

Z-Score

6.786
7.21
8.386
14/15 subjects

6.895
3.191
6.32
5.945
7.57
4.916
4.202
7.427
7.335
6.343
6.983

Z-Score15/15 subjects

Right Clench Area Talairach⫺12.14 ⫾ 3.84

44.87
40.83
35.63
33.85
38.49
36.43
34.78
37.71
33.54
36.6
37.12
38.12
40.31
37.03
40.06
34.17
35.56
35.66

⫺14.86⫺12.01⫺6.14⫺11.31⫺9.21⫺11.9⫺13.57⫺12.03⫺13.39⫺9.67⫺11.15⫺12.43⫺10.35⫺15.61⫺6.49⫺14.79⫺16.09⫺21.54yx46.97 ⫾ 4.91

38.91
51.92
51.74
41.45
45.28
49.29
37.78
43.69
40.42
44.29
49.53
49.05
55.53
41.4
52.13
42.66
41.83
48.25

z

y

102
194
29

205
72
168
28
196
165
46
159
216
257
247

No. ofVoxels

166
140
276
71
224
198
89
211
103
135
146
189
49
90
107
110
75
158

No. ofVoxels

⫺15.49⫺8.1⫺19.98⫺10.49 ⫾ 6.16

⫺7.28
⫺4.75
⫺7.57
⫺5.97
⫺10.06⫺5.43⫺14.54⫺6.59⫺24.19⫺59.29⫺60.76⫺56.17⫺59.83⫺44.4⫺60.23⫺46.71⫺58.21⫺55.28y⫺6.4⫺63.36⫺59.68⫺61.92⫺57.21 ⫾ 5.62

36.13 ⫾ 2.39

37.8
36.64
36.2
36.23
36.4
38.61
36.19
38.37
37.81
35.67
34.19
37.09
32.6
35.94
37.39
37.21
36.34
29.56

z

28.4
23.41
12.77
25.98 ⫾ 9.14

29.26
29.97
32.3
35.72
29.83
29.62
2.03
24.53
33.02

26.88

z

9.365
6.83
7.974
7.883
7.785
9.51
9.872
8.495
9.315
8.123
15.14
5.673
5.911
5.532
4.464
7.534
6.822
10.832Z-Score

7.552
6.844
8.978
13/15 subjects

6.005
6.309
8.262
5.307
4.299
7.409
8.333
6.147
6.851

6.385

Z-Score15/15 subjects

Left Clench Area Talairach⫺14.59 ⫾ 3.73

⫺16.96⫺13.39⫺10.74⫺14.03⫺13.8⫺16.44⫺17.64⫺12.9⫺13.65⫺17.16⫺18.95⫺10.21⫺15.35⫺13.26⫺7.87⫺13.88⫺14.35⫺23.18y⫺57.86x⫺50.63 ⫾ 4.87

⫺48.73⫺58.3⫺59.96⫺50.8⫺50.7⫺50.44⫺45.31⫺51.69⫺46.12⫺43.25⫺53.03⫺43.52⫺47.73⫺54.81⫺55.53⫺49⫺47.96⫺53.53x

Left Smile Area Talairach

258
134
194

381
89
345
174
52
145
266
99
146

148

No. ofVoxels

316
246
46
30
10
156
200
218
301
83
370
163
204
362
112
24
150
45

No. ofVoxels*A significant smile– clench difference was clearly observed in 15 participants in the right and left middle precentral gyrus. Three participants also showed significant differences in the bottom
region of right and left precentral gyrus (S3, S5, and S11, shown as italic). Fourteen participants presented significant differences in the lower region of the precentral gyrus in right hemispheresfor clench–smile contraction. In the left hemisphere, 13 participants showed a similar significant pattern over the lower region of the precentral gyrus.

S1
S2
S3
S4
S5
S6
S7
S8
S9
S10
S11
S12
S13
S14
S15
Mean ⫾ SE

Mean ⫾ SE

S12
S13
S14
S15

S6
S7
S8
S9
S10
S11

S4
S5

S1
S2
S3

x

Right Smile Area Talairach

Table 1. Mean Coordinate Level of Activation and Size of the Functional Regions Observed in All Participants*

Plastic and Reconstructive Surgery • April 2013

Volume 131, Number 4 • Identifying Areas of Facial Function

Fig. 1. Group t map showing areas in which significant increases in blood
oxygen level– dependent activation responded to smile (upper) andclench (lower). The coordinates of the smile region are 43, ⫺12, 37 (right,
Z ⫽ 18.291, size ⫽ 277 voxels) and ⫺48, ⫺13, 38 (left, Z ⫽ 18.113, size ⫽302 voxels). The coordinates of the clench region are 59, ⫺4, 30 (right,
Z ⫽ 11.321, size ⫽ 254 voxels) and ⫺59, ⫺6, 32 (left, Z ⫽ 10.913, size ⫽ 66
voxels).

Fig. 2. Schematic representation on two Talairach slices (y ⫽ ⫺9 and ⫺13)of the areas of activation in the precentral gyrus for smile and clench.

and left precentral gyrus (see Table 1, participants
S3, S5, and S11, whose values are shown in italics).
The mean coordinates for this secondary smile region were 39, –13, 35 (right, mean Z ⫽ 7.449, mean
size ⫽ 83 voxels) and – 49, 15, 35 (left, mean Z ⫽7.762, size ⫽ 197 voxels).

DISCUSSION
The mechanism of cerebral cortical reorganization is not well established in facial reanimation
patients. Specifically, whether a truly spontaneousand emotional smile is achievable using neural
input from a nonfacial nerve is still open to debate.

531e

Plastic and Reconstructive Surgery • April 2013
Surgical techniques using either the facial or thetrigeminal nerve can lead to fairly symmetricalfacial movement with regard to smiling. However,a myriad of techniques are commonly used, andwhich of these leads to better and more natural
results is still currently debated.
The successful use of functional magnetic resonance imaging to differentiate between neural activity of the facial and trigeminal nerves has promising implications in determining the nature ofcortical reorganization in facial reanimation. This isimportant, as it provides an objective measure ofbrain plasticity between groups of patients who have
had reanimation using both facial and trigeminal
nerve donors. Moreover, the reliable spatial resolution provided by functional magnetic resonance imaging promises to resolve the controversy surrounding trigeminal donor reanimation (either nerve to
masseter or temporalis transfer), namely, whether
this technique can truly lead to a spontaneous smilein the absence of teeth clenching.25
When Zuker et al. introduced the use of the
motor branch to the masseter muscle, a branch of
the trigeminal, to activate segmental gracilis muscle
transplants in facial reanimation children with Möbius syndrome, they concluded that a fully spontaneous smile was not achievable.7 However, in 2011,
Schaverien et al., performing electromyography ofthe masseter muscle in patients with free gracilis–
to–masseter nerve transfer, showed a natural contraction of the masseter muscle during normal smile
occurring in 50 percent of their subjects.25 The phenomenon of patients achieving a spontaneous smile
following free gracilis–to–masseter nerve transfer isanother sign of brain plasticity. With practice, patients can develop the ability to smile spontaneously
and without jaw movement.8
Ziemann et al. showed in study of the modulation of practice-dependent plasticity in human motor cortex that motor practice leads to expansion oftrained representations in the motor cortex,26 probably because of the preexisting but latent horizontal
connections in the cortex. One explanation for thedevelopment of a spontaneous smile following theuse of a trigeminal motor nerve is if, for example, afree gracilis–to–masseter nerve transfer inducedchange in cortical motor reorganization through theuse of preexisting but latent horizontal connectionsin the cortex. In this scenario, there could be thepotential for a spontaneous smile without jaw movement. The successful use of functional magnetic resonance imaging to differentiate between activities in
the facial nerve–related cortex activating a smile andthe trigeminal cortex activating teeth clenching isable to provide a satisfactory answer to this question.

532e

One previous study has looked at functional
magnetic resonance imaging in smile generationand successfully demonstrated a distinct corticalarea relating to smile generation.27 Talairach coordinates found in this study generally correlate
well with those seen in our study.
Importantly, we did not aim to isolate the neuraldifferences between voluntary and involuntary
smile. This is to date an extremely controversial
topic, with some authors28 arguing for the existenceof different pathways of activation for the two typesof smile, others29 reporting no difference between
them, and a final strand claiming that cultural andsocial influence render cortical activations following
voluntary or involuntary smile unpredictable.30 However, based on current knowledge, we can confidently state that the brain regions isolated here account for only the motor component of smiling,which represents the final stage of this process, and
it is thus well beyond this dichotomy.30 Whether asmile is voluntary or involuntary would indeed produce differential neural patterns. This difference,
however, would affect only subcortical regions (suchas the amygdala) or regions involved in emotional
evaluations. Crucially, both types of neural patterns
elicited by involuntary and voluntary smile would
trigger neural activity in the same motor-corticalarea, responsible only for producing the movementof a smile (which is the same regardless of the cause).
Therefore, this difference will not impact on thelocation and the activation for the smile we found
here.

CONCLUSIONSFor the first time, we show that there are two
distinct cortical areas subserving smiling and teeth
clenching. This result allows an objective assessment of cortical reorganization between groups of
facial and trigeminal nerve donor reanimation patients. Having successfully and consistently identified these two cortical areas by investigating thevariations in blood oxygen level– dependent signal
activity among them, we can finally assess the extent and nature of cortical reorganization. The
latter has been shown to occur in clinical settings
such as Braille reading,18 limb amputation,19,20 andnerve injuries31 and thus is likely to also occur infacial reanimation patients. In the future, it will bepossible to follow any changes in cortical activity
directly related to brain plasticity as patients recover following facial reanimation surgery using
either the facial nerve or trigeminal nerve
branches as a motor. This will allow surgeons toadvise patients regarding the likelihood of devel-

Volume 131, Number 4 • Identifying Areas of Facial Function
oping a spontaneous smile using different techniques of facial reanimation.
Marco Romeo, M.D.
Canniesburn Plastic Surgery Unit
Glasgow Royal Infirmary
84 Castle Street
G4 DSF Glasgow, Scotland
romeoplastica@gmail.com

ACKNOWLEDGMENT

Junpeg Lao received a grant by the CanniesburnResearch Trust for the work done during article development.
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