Japanese Dental Science Review (2010) 46, 132—142

a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m

journal homepage: www.elsevier.com/locate/jdsr

Review article

Neuroplasticity of face sensorimotor cortex and

implications for control of orofacial movements
Limor Avivi-Arber a,b, Jye-Chang Lee b, Dongyuan Yao b, Kazunori Adachi b,1,
Barry J. Sessle b,*

a
Department of Prosthodontics, Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada
b
Department of Oral Physiology, Faculty of Dentistry, University of Toronto, 124 Edward St., Toronto, Ontario M5G 1G6, Canada

Received 31 October 2009; received in revised form 30 November 2009; accepted 30 November 2009

KEYWORDS Summary The vast and complex array of orofacial muscles and movements necessitate
Orofacial; sophisticated and adaptive neural circuits providing for their control and integration with other
Motor control; motor behaviours. It has become apparent from anatomical, electrophysiological, imaging and
Somatosensory; behavioural studies of the face sensorimotor cortex in humans or laboratory animals that the face
Neuroplasticity; primary motor cortex (MI) and the face primary somatosensory cortex (SI) make important
Muscles contributions not only to the control of elemental and learned orofacial movements but also to
mastication and swallowing that in the past have been largely attributed to brainstem regulatory
mechanisms. Recent studies have also documented that neuroplastic changes occur in face
sensorimotor cortex following intraoral alterations (e.g., noxious stimulation, dental occlusal
changes, nerve trauma) and in association with oral motor skill acquisition, and appear to reflect
dynamic and adaptive events modelled by behaviourally significant experiences, including pain
and other alterations to the oral environment. Further elucidation of the role and neuroplasticity
of the face sensorimotor cortex in relation to orofacial motor control, as well as the intracortical
mechanisms underlying the neuroplasticity, hold promise of new insights that are critical for
developing improved rehabilitative strategies to exploit these mechanisms in humans suffering
from chronic pain or sensorimotor disorders.
# 2009 Japanese Association for Dental Science. Published by Elsevier Ireland. All rights reserved.

Contents

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
2. Overview of orofacial sensorimotor circuits and role of face sensorimotor cortex . . . . . . . . . . . . . . . . . . . . . . . . 133

* Corresponding author. Tel.: +1 416 979 4921x4336; fax: +1 416 979 4936.
E-mail addresses: barry.sessle@utoronto.ca, limor.avivi.arber@utoronto.ca (B.J. Sessle).
1
Present address: Department of Diagnostic & Therapeutic Sciences, Division of Pharmacology, Meikai University School of Dentistry,
Saitama, Japan.

1882-7616/$ — see front matter # 2009 Japanese Association for Dental Science. Published by Elsevier Ireland. All rights reserved.
doi:10.1016/j.jdsr.2009.11.007
Neuroplasticity of face sensorimotor cortex 133

3. Neuroplasticity of face sensorimotor cortex. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135

3.1. General considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
3.2. Orofacial alterations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
3.2.1. Face SI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
3.2.2. Face MI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136
3.3. Orofacial motor skill acquisition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137
3.3.1. Face SI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
3.3.2. Face MI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
4. Clinical implications. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139

1. Introduction include the intertrigeminal nucleus, supratrigeminal

nucleus, and certain parts of the brainstem reticular forma-
Over the past 30 years, there have been considerable tion. The main cranial nerve motor nuclei involved in orofa-
advances in understanding the peripheral and central neural cial movements include the Vth motor nucleus that supplies
mechanisms underlying the initiation and regulation of motor most jaw muscles, the VIIth motor nucleus that provides the
functions. The literature on motor control has especially motor innervations of the muscles of facial expression, the
focussed on the control of limb motor functions, and indeed nucleus ambiguus that mainly supplies muscles of the palate,
reviews of the topic of motor control have often completely larynx and pharynx, and the XIIth motor nucleus supplying the
neglected the topic of orofacial motor control. Yet many extrinsic and intrinsic tongue muscles.
orofacial movements necessitate exquisite motor control These interneuronal and motoneuronal sites receive and
processes to coordinate the activity of the vast array of process afferent inputs not only from various orofacial tissues
muscles in the orofacial region. The various mammalian but also from other brainstem and suprabulbar areas.
muscles involved in orofacial motor function serve important Thereby they provide neural circuits and processes that
and diverse functions, some of which are crucial for sustain- are involved in initiating or modulating orofacial reflexes
ing the very life of the animal. In addition, there are unique and other motor functions (see Refs. [1,2,4,5]). Some of
characteristics of the orofacial motor system that distinguish these neural circuits and processes may also be elements
it from the (spinal) motor system that controls the muscles of of the central programs (pattern generators) that are so
the limb, trunk and neck (see Refs. [1—3]). It has become crucial in the initiation and control of complex functions
evident that the so-called sensorimotor region of the cere- such as swallowing and chewing. In addition to their role in
bral cortex is a vital element in the regulation and sensor- the brainstem interneuronal circuits, the trigeminal brain-
imotor coordination of the orofacial muscles. This review will stem sensory nuclear complex and the solitary tract nucleus
focus on the neuroplasticity of the sensorimotor cortex in also relay orofacial sensory information from the brainstem
relation to the acquisition of motor skills and adaptation to to several higher brain areas. These areas are involved in
alterations to the oral environment. perceptual and cognitive processes related to orofacial sen-
sations or in sensorimotor control of the orofacial muscles.
Several of these areas project directly or indirectly (e.g., via
2. Overview of orofacial sensorimotor the interneuronal sites) to the cranial nerve motor nuclei
circuits and role of face sensorimotor cortex and, as noted above, can thereby exert modulatory influ-
ences on orofacial motor activities. Such an area is the so-
Muscles in the orofacial region may be guided in their dif- called face sensorimotor cortex and it will be the focus of the
ferent functions by sensory inputs to their motoneurons that remainder of this review.
derive from a large array of different types of sense organs The face sensorimotor cortex includes the face primary
(receptors) in the orofacial region. These receptors include somatosensory area (SI) and the face primary motor area (MI)
mechanoreceptors, proprioceptors, thermoreceptors, noci- that have distinct cytoarchitectonic features. For example,
ceptors, gustatory and other chemoreceptors (see Refs. the sensorimotor cortex has several layers, and the SI is
[1,2,4,5]). The primary afferents associated with these characterized by a granular layer IV that is the main cortical
receptors have their cell bodies in the trigeminal or other area receiving bilateral orofacial inputs relayed through the
cranial nerve ganglia, and most of the somatosensory affer- thalamic somatosensory nuclei. In contrast, MI lacks a pro-
ents project to the trigeminal brainstem sensory nuclear minent granular layer IV and has large pyramidal cells within
complex. The solitary tract nucleus in the caudal brainstem layer V that project to other cortical areas as well as supra-
receives visceral afferents (e.g., those supplying lingual taste bulbar and brainstem motoneuronal and interneuronal
buds, laryngeal and pharyngeal taste buds and mechanore- regions involved in orofacial motor control (see above). SI
ceptors). There are extensive projections from these two is principally involved in somatosensation and manifests a
sensory nuclear regions to the cranial nerve motor nuclei. topographic arrangement of the body, with the orofacial
Thus, these two regions are the sites of neurons relaying region (face SI) represented in its most lateral aspect. MI
sensory information from the orofacial receptors to the also is organized topographically, with face MI located most
motoneurons in these motor nuclei. Other brainstem inter- laterally in MI. However, it is now evident that face SI, like
neuronal sites involved in orofacial sensorimotor functions face MI, has a role in sensorimotor integration and control.
134 L. Avivi-Arber et al.

This evidence includes (i) the extensive connections between vital role in the generation and control of voluntary elemen-
face SI and MI, (ii) motor outputs from SI as well as MI to tal as well as semiautomatic and rhythmic orofacial motor
brainstem regions involved in motor as well as somatosensory functions. For example, in awake monkeys, short-train intra-
functions, and (iii) the SI and MI neuronal motor-related cortical microstimulation (ICMS) can evoke elemental move-
activity patterns and motor effects of SI or MI stimulation ments such as jaw opening and tongue protrusion when
or lesions (see Refs. [2,6—10]) as noted below. applied to face MI [19—25] (Fig. 1). Short-train ICMS can also
Orofacial motor dysfunctions such as dysphagia, dysar- evoke jaw and tongue movements when applied to the face SI
thria, impaired mastication and drooling are common clinical or face MI in subprimates [26—31]. On the other hand, long-
occurrences associated with sensorimotor cortex lesions train ICMS can evoke semiautomatic movements such as
(e.g., a stroke) and with altered sensory inputs such as those mastication, swallowing and facial whisking from the face
resulting from peripheral nerve damage (see Refs. [6,10,11]). MI and face SI of monkeys and subprimates [19—22,32—34].
These clinical observations suggest that cortical mechanisms Single neuron recordings reveal that neurons within many of
involving sensorimotor integration may be critical for the the ICMS-defined face SI as well as face MI sites show activity
generation and control of orofacial movements. A variety of related to mastication and swallowing and/or to a trained
techniques used in humans have also confirmed the impor- jaw-closing or tongue-protrusive task in monkeys, and to
tance of the face SI and MI in orofacial motor control. These mastication, licking and whisking in rats and cats [9,23—
include transcranial magnetic stimulation (TMS), functional 25,33,35—39]. Also, neurons in face MI as well as face SI
magnetic resonance imaging (fMRI), magnetoencephalogra- may have an orofacial mechanoreceptive field from which
phy and stimulus-evoked potentials. For example, TMS of they can be activated (e.g., by tactile stimulation)
face MI can activate one or more orofacial muscles from an [19,21,23,26,35,38,40]. Furthermore, there tends to be a
extensive area within face MI, and fMRI has revealed that close spatial matching of orofacial somatosensory afferent
semiautomatic (e.g., swallowing) as well as elemental (e.g., inputs and motor output effects at face MI microzones repre-
tongue protrusion, jaw opening) movements and even ima- senting a particular orofacial muscle [19,21,23,26]. Addition-
gery of voluntary orofacial movements involves activation of ally, cold block or lesioning of the ICMS-defined face MI may
face SI as well as face MI (and other cortical areas) [12—18]. modify mastication and masticatory-related jaw and tongue
These findings in humans are consistent with studies in EMG activities and may also impair the animal’s ability to
animals indicating that the face MI as well as face SI have a perform a tongue-protrusion task but has limited effects on

Figure 1 (A) Distribution of rhythmic jaw movement (RJM) sites evoked by short- and long-train ICMS within the monkey ‘‘unfolded’’
right face MI and the more lateral pericentral cortex. 0 mm, top of the rostral bank of the central sulcus; dashed line on the right
represents the bottom of the central sulcus. (B) Diagram showing the approximate location (— — —) of the implanted cylinder that
allowed access of the microelectrode used for applying ICMS. (C) ‘‘Folded’’ pericentral cortex. Arc: Arcuate sulcus. Cen: central sulcus.
RJMi–—ipsilateral, RJMv–—vertical, RJMc–—contralateral and ICMS–—intracortical microstimulation (adapted from Ref. [20]).
Neuroplasticity of face sensorimotor cortex 135

the animal’s ability to perform a learned biting task and tor cortex following alterations to intraoral tissues and sen-
swallowing per se [34,41—47]. Likewise, cold block or sory inputs and in the acquisition of novel orofacial motor
lesioning of face SI interferes with the animal’s ability to skills. It should be noted however that sensorimotor cortex
perform a tongue-protrusion task but has limited effects on neuroplasticity can also occur during development [54,69,70]
the biting task, swallowing and masticatory functions and as a result of CNS lesions such as stroke that can lead to
[29,41,48—50]. marked cognitive and physical disabilities [10,71]. However,
These various findings from studies in humans and labora- such considerations are beyond the scope of this present
tory animals emphasize the crucial role played by both face SI review.
and face MI in the generation and control of orofacial motor
functions. They also emphasize the significance of the exten- 3.2. Orofacial alterations
sive somatosensory input from the orofacial region in the fine
control, coordination and modulation of the orofacial motor 3.2.1. Face SI
activities, including mastication and swallowing that in the Alterations to or deafferentation or deefferentation of oro-
past have been attributed largely to brainstem regulatory facial sites may induce neuroplastic changes of the somato-
mechanisms. sensory representations within face SI. Such changes may
occur early in development and throughout life, suggesting a
role for face SI in experience-dependent development and
3. Neuroplasticity of face sensorimotor
adaptive processes in adulthood (see Refs. [68,72—75]). In
cortex humans, SI reorganization may occur in several chronic pain
conditions [62,76,77]. For example, brain imaging studies
3.1. General considerations have revealed that limb amputation may be associated with a
significant expansion of face somatosensory representations
Neuroplasticity in the context of this review refers to the into the neighbouring SI area represented by the deprived
ability of the sensorimotor cortex to undergo structural and limb. This reorganization is often seen in phantom limb pain
functional changes throughout life. These neuroplastic and a daily use of a myoelectric prosthesis in these patients
changes represent crucial processes for numerous brain func- may be associated with reduced cortical reorganization and
tions. These functions include cognition, memory, motor skill less phantom limb pain. Edentulous patients treated with
acquisition, perceptual learning, and adaptation following implant-supported prostheses report improved tactile dis-
damage to CNS structures (e.g., by stroke) or alterations to criminative capabilities, increased biting forces and
peripheral tissues or nerves that modify sensory inputs to the improved motor functions (e.g., [78,79]). Furthermore, a
CNS (e.g., [51—57]). Neuroplasticity and related behavioural recent fMRI study has reported that in comparison with
changes may not only reflect adaptive modifications that are edentulous patients treated with conventional complete
beneficial but could instead represent maladaptive modifica- dentures, edentulous patients treated with implant-sup-
tions that result in impaired function. ported prostheses show significantly increased activity within
The mechanisms underlying such neuroplastic changes face SI [80]. This finding suggests a possible role of face SI in
involve several intracortical neurochemical changes (e.g., patients’ adaptation (or lack of adaptation) to their dental
in acetylcholine, GABA, norepinephrine, glutamate) (e.g., prostheses.
[51,52,58—63]). Rapid neuroplastic changes can occur within In laboratory animals such as rats which use their vibrissae
minutes and may be explained by mechanisms such as altered for tactile exploration of their environment, the neuroplas-
synaptic efficiency or unmasking (e.g., through disinhibition) ticity of the rodent barrel cortex in face SI has been the focus
of existing intracortical excitatory synaptic connections of considerable research. For example, altered somatosen-
which are usually ineffective because of inter- and intra- sory experience in neonatal or fetal rats can be produced by
hemispheric lateral inhibition. Mechanisms involved in facial nerve transection, vibrissal trimming or lesioning,
longer-lasting changes include enhanced gene expression, perioral noxious stimulation or anaesthetic block, or transec-
axon sprouting and dendritic branching and synaptogenesis tion of the infraorbital nerve (supplying sensory innervation
and may involve cortical volume changes. Long-term poten- to the vibrissae). These peripheral alterations can induce
tiation may play a role at early as well as late phases of the anatomical and functional changes within the barrel cortex
neuroplastic process (i.e., vibrissal SI) of adult rats. These include changes in
In limb SI and MI of subprimates and primates, neuroplas- mechanoreceptive field properties of vibrissal-related neu-
tic changes can be induced by trauma (i.e., transection) of rons and somatotopic reorganization whereby the SI region
peripheral sensory or motor nerves or manipulations of sen- representing adjacent vibrissae expands into the region
sory inputs or motor functions (see Refs. [52—54,64]). Neu- representing the deprived or trimmed vibrissae (see Refs.
roplastic changes in limb SI and MI are also evident during [52,54,64]). More permanent peripheral intraoral deaffer-
development when an infant encounters novel sensory and entation induced by extraction of a mandibular incisor in
motor experiences as he or she learns and acquires new young adult mole-rats results, 5—8 months later, in functional
motor skills (e.g., walking). Neuroplasticity also occurs dur- reorganization of face SI. This reorganization is manifested as
ing adulthood when a person learns for example to play a the entire extent of the deprived incisor somatosensory
musical instrument or a sport or develop a particular surgical representation becoming represented by other orofacial tis-
skill. On the other hand, non-skilled limb training has been sues ([123], Fig. 2). There is a small orofacial motor repre-
associated with a lack of cortical reorganization of motor sentation within the rat face SI, and this motor
representations (see Refs. [53,64—68]). This section of the representation is also subject to neuroplastic changes since
review focuses on the neuroplasticity of the face sensorimo- mandibular incisor extraction is associated 1 week later with
136 L. Avivi-Arber et al.

Figure 2 (A) Somatosensory representation map of the body parts within SI of a mole-rat. Dots represent individual electrode
penetration sites. Star indicates electrolytic lesion site. X indicates a non-responsive site. C is a higher magnification of B, 5 months
following mandibular incisor extraction, illustrating the expansion of the tongue, ipsilateral incisor and other neighbouring
somatosensory representations into the SI area previously represented by the deprived incisor (adapted from Ref. [123]).

a significant increase in the representation of the anterior neonate CNS (e.g., vibrissal trimming, infraorbital nerve
digastric muscle [31,81]. injury) or lesioning the facial nerve that provides the motor
supply to the vibrissal muscles results in a reduction in the
3.2.2. Face MI vibrissal representation or excitability and an expansion of
Deefferentation is also associated with face MI neuroplasticity. the adjacent forelimb representation in MI [52—54,100,101].
For example, patients with facial muscle paralysis have been While it has been reported that partial trigeminal deaffer-
reported to show expansion of the TMS-defined hand repre- entation is not associated 16 days later with any significant
sentation into the face MI [82—84]. Human TMS studies indi- changes in the more lateral so-called cortical masticatory
cate that changes also occur in face MI following a transient area (CMA) in rabbits [102], recent ICMS studies have pro-
deafferentation (produced by local anaesthesia) of orofacial vided evidence of face MI neuroplasticity following intraoral
areas [85—87] or pharyngeal stimulation [10,88]. Pain is manipulations. These recent studies were driven in part by
another sensory experience that may induce MI neuroplasti- clinical observations that adaptive behaviours occur when
city. Several pain-related changes in motor behaviour involve the dental occlusion is modified or intraoral (e.g., lingual)
local segmental or brainstem reflex circuits, but there is nerves damaged, and in some cases maladaptive behaviours
growing evidence of the involvement of higher central nervous may result [8,31,81,103]. Unilateral transection of the lin-
system centres such as the sensorimotor cortex. For example, gual nerve supplying sensory innervation to the rat’s tongue
in humans, decreased limb MI excitability may be associated results in significant time-dependent changes of the anterior
with chronic pain states such as phantom limb pain or with digastric and genioglossus representations within face MI, 1—
experimentally induced cutaneous or muscle pain [62,89—92]. 4 weeks later [103]. In addition, extraction of a mandibular
Face MI excitability has been reported in TMS studies in humans incisor in rats is associated 1 week later with significant
to be unaffected by capsaicin-induced facial or lingual pain or neuroplastic changes within the contralateral face MI that
hypertonic saline-induced masseter muscle pain [86,93]. How- are manifested as a significant expansion of the ICMS-defined
ever, Boudreau et al. [94] documented that capsaicin-induced anterior digastric motor representation (Table 1) [8,31].
intraoral pain interferes both with successful performance by Trimming both rat mandibular incisors also induces face MI
humans of a novel tongue-protrusion task and with tongue MI neuroplastic changes but this is reflected as a significant
neuroplastic changes associated with successful performance reduction in the anterior digastric representation in face
of the task, consistent with rat data (Fig. 3; also see below). MI that can be restored if the incisors are allowed to erupt
There are also reports of MI excitability changes or reorganiza- back into occlusion [8]. This latter finding is consistent with
tion in several chronic pain states (e.g., [62,76,95—99]). findings of face MI neuroplasticity with vibrissal trimming and
Animal studies have also revealed MI neuroplasticity fol- regrowth [104] (Table 1).
lowing orofacial manipulations, including acute noxious sti- In the case of animal models of acute orofacial pain, many
mulation. Altering the vibrissal afferent input to the adult or studies in awake or anaesthetised animals have shown that
Neuroplasticity of face sensorimotor cortex 137

Figure 3 The effects of the algesic chemical capsaicin applied to the intraoral region on learned tongue-task performance and face
MI excitability in humans. A shows the mean tongue-protrusion trial performance scores (expressed as %performance) for all subjects
with respect to tongue task trials with a control vehicle or capsaicin. B and C are TMS—MEP stimulus—response curves elicited from the
tongue MI of all 9 subjects; B for the vehicle tongue-protrusion training sessions which shows a significant enhancement between the
pre- and post-training MEPs and C for the capsaicin tongue-protrusion training sessions which shows no significant differences between
the pre- and post-training MEPs. Significant differences are indicated by asterisks, and data are presented as means  SEM (TMS–—
transcranial magnetic stimulation and MEP–—motor-evoked potential) (adapted from Ref. [94]).

acute noxious orofacial stimulation induces or modifies motor stimulus site. The finding is consistent with earlier findings of
behaviour [1,2,5]. Cortical changes may be involved in such close input—output coupling for the tongue MI representation
behavioural changes since significantly increased ICMS [21,23,24]. The finding also suggests that the dental extrac-
thresholds for the tongue (genioglossus) motor representa- tion effects on face MI (see above) were unlikely due to pain
tion occur in face MI for several hours after acute noxious since, in contrast to the extraction-induced increased repre-
stimulation of the rat tongue [105]. This effect is primarily sentation, noxious lingual stimulation produced a decreased
reflected intracortical changes and specifically targets motor MI excitability [103].
outputs to the region (tongue) in the vicinity of the noxious The neuroplastic changes associated with alterations to
teeth or lingual sensory function could conceivably result
from a sensorimotor behaviour that the animal has modified
Table 1 Summary of the number of positive ICMS sites to adapt to the altered intraoral state. Another possibility is
within the left face MI from which EMG activity could be that the changes are the result of alterations in sensory
evoked in jaw and tongue muscles 1 week following trimming inputs to the sensorimotor cortex that then allow the animal
the two mandibular incisors (incisors trimming group), ex- to adapt its behaviour to the modified intraoral state. The
traction of the right mandibular incisor (incisor extraction design of most experiments addressing the neuroplastic
group) or transection of right lingual nerve (nerve transection effects in sensorimotor cortex of peripheral manipulations
group). In comparison with the naı̈ve control groups, bilateral has not allowed for a clear distinction of these two possibi-
incisor trimming resulted in a significant decrease in the lities. However, most of the literature (see above) on MI
number of LAD and RAD positive ICMS sites; unilateral incisor neuroplasticity and motor control suggests the latter possi-
extraction resulted in a significant increase in the number of bility and supports the view that MI neuroplasticity reflects
RAD sites; and unilateral nerve transection resulted in a dynamic, adaptive constructs responsive to changes in the
significant decrease in the number of RAD and GG positive sensory environment [106—108]. The neuroplasticity is also
ICMS sites. viewed as underlying the animal’s ability to learn new motor
Experimental group Muscle Positive ICMS sites skills or adapt its motor behaviour as it adjusts to the altered
(mean  SEM) peripheral state. Furthermore, it is considered that MI is
specifically engaged during the acquisition phase of novel
Incisors trimming LAD 71.5  9.6 * motor skills, and that the associated neuroplasticity is not the
RAD 62.0  8.1 * result of increased muscle or nerve excitability. The view
GG 67.9  13.5 that the MI neuroplastic changes are crucial for the adapta-
tion and acquisition of new motor skills and behaviour appro-
Incisor extraction LAD 145.6  17.6
priate to the altered sensory environments is consistent with
RAD 150.9  20.4 *
recent evidence for neuroplasticity of face sensorimotor
GG 100.7  22.3
cortex in association with learning of novel orofacial motor
Nerve transection LAD 78.9  15.5 skills, as noted below.
RAD 74.4  10.4 *
GG 46.0  11.7 ** 3.3. Orofacial motor skill acquisition
LAD–—left anterior digastric; RAD–—right anterior digastric and Although cortical neuroplasticity as it relates to orofacial
GG–—genioglossus.
* motor skill acquisition has not been extensively studied,
p < 0.05.
** clinical reports suggest that neuroplasticity or progressive
p < 0.01 (ANOVA followed by post hoc tests).
return of function of face sensorimotor cortex can occur
138 L. Avivi-Arber et al.

following cortical damage or manipulations of orofacial sen- acquired needs direct testing, e.g., in animals. Unfortu-
sory inputs (see Refs. [6,10,51,52,109,110]). There is also nately, animal studies of face MI neuroplasticity related to
evidence of such neuroplasticity from some recent experi- motor skill acquisition are sparse. It has recently been
mental studies in humans and laboratory animals, as outlined reported in rats that tongue force training alone does not
below. produce lasting changes in the size of the orofacial cortical
motor representation in face MI but does decrease the
3.3.1. Face SI current thresholds necessary for eliciting an ICMS-evoked
Many studies have shown that the functional organization and tongue motor response [119]. The possible neuroplasticity
neuronal properties of limb SI can undergo neuroplastic of face MI (and SI and CMA/swallow cortex) has recently been
changes in association with a motor skill acquisition and that explored in awake monkeys over a 1—2-month period before,
these changes may depend on experience and context (see and again after, a 2—6-week period of their training in a novel
Refs. [111,112]). Analogous studies of face SI in humans are tongue-protrusion task [8]. Compared with pre-training data
lacking. However, training awake monkeys in a novel tongue- in trained animals and data in control untrained animals, the
protrusion task may result in increased proportions of face SI trained animals showed evidence of neuroplastic changes.
neurons having lingual mechanosensory inputs and manifest- There was a significant increase in the proportion of discrete
ing tongue protrusion-related activity [8,113]. In addition, ICMS-defined MI efferent microzones for tongue protrusion
consistent with the Hebbian concept of differential-use neu- and a decrease in zones for lateral tongue movement, and
roplasticity [114], increases in behaviorally relevant inputs significant increases in the proportions of neurons in MI (and
from spared or trained vibrissae result in increased repre- SI; see above) showing tongue protrusion-related activity and
sentation of the spared vibrissae within the rodent barrel lingual mechanosensory inputs. Such findings are consistent
cortex (see Refs. [54,64]). For example, trimming of rat with the documentation of changes in limb MI neuronal
vibrissae results in changes in exploratory motor behaviour properties during the learning of a motor task (see Refs.
by the rat that favours the use of the untrimmed vibrissae [52,57,120]). Interestingly, changes analogous to those in
[115]. In addition, as mentioned above, vibrissal trimming face MI (and SI) were not apparent in CMA/swallow cortex
can be associated with an increase in the representation of [8]. This finding suggests a degree of specificity in that a
non-trimmed adjacent vibrissae within the barrel cortex. differential expression of task-related neuroplasticity may
Such reorganization may also occur faster when rats are occur in these three cortical areas.
placed in an environment enriched with novel objects and
many other rats [116]. In addition, training rats left with only 4. Clinical implications
three adjacent vibrissae in a tactile discrimination task
results in barrel cortex reorganization reflected in a signifi- The neuroplastic capabilities of the face sensorimotor cortex
cantly increased representation of the behaviourally that have been outlined above may reflect or allow for
engaged vibrissae [117]. functional adaptation (or maladaptation) of the masticatory
system to an altered oral state or altered oral motor beha-
3.3.2. Face MI viour. They may contribute to the mechanisms whereby
Studies using transcranial magnetic stimulation (TMS) have patients undergoing oral rehabilitation can (or cannot)
shown that training humans for less than 1 h in a novel restore the lost orofacial sensorimotor functions. This infor-
tongue-protrusion task (analogous to that used for studying mation is important since pain, injuries to the oral tissues,
face MI neuroplasticity in monkeys; see below) results in a and modifications to the dental occlusion induced by tooth
significantly increased tongue representation within face MI, loss or attrition are common occurrences in humans that may
decreased TMS-evoked thresholds and increased amplitude sometimes be accompanied by impaired oral sensorimotor
of TMS-evoked tongue motor potentials [16,17]. These neu- functions. Furthermore, impaired oral motor functions are
roplastic changes are associated with significantly improved common in many neurological disorders (e.g., brain injury,
successful task performance. However, training may not be stroke, Parkinson disease). Such impairment can sometimes
associated with changes in intra-cortical inhibitory or facil- make the most vital functions of eating, swallowing and
itatory networks [118]. Sensory perturbation induced by speaking difficult and thereby reducing the patient’s quality
experimental intraoral noxious stimulation concomitantly of life [2,11,121,122]. Therefore, understanding the
prevents both successful tongue-task performance and the mechanisms and cortical neuroplastic processes underlying
increased tongue-MI excitability associated with the task orofacial sensorimotor functions and adaptation is important
training (Fig. 3) [94]. However, sensory deprivation induced for the development of new treatment strategies to facilitate
by topical anaesthesia of the tongue is reported to have no recovery of such patients suffering from orofacial pain con-
acute effect on face MI excitability [87]. The close correla- ditions and sensorimotor deficits and improve their quality of
tion between successful task performance and the rapid life. Indeed, in recent years, based on animal and human
onset of MI neuroplasticity suggests that the tongue MI study models, principles of sensorimotor cortex neuroplas-
changes reflect events that are necessary for achieving high ticity have been translated into novel evidence-based prac-
performance in the task. This view is in keeping with the tices. These include inducing cortical neuroplasticity or
principle of the positive influence of cortical neuroplasticity reversing undesirable neuroplastic changes in order to
‘‘use it and improve it’’ [67]. enhance the effectiveness of rehabilitative approaches in
The dynamic features and rapid appearance of neuroplas- patients suffering from chronic pain or sensorimotor disor-
ticity in the above human studies suggesting that neuroplas- ders [10,56,57,75,110]. Regrettably these principles, parti-
tic changes are likely occurring in the face sensorimotor cularly as they relate to face sensorimotor cortex and
cortex neurons as the novel orofacial motor skill is being orofacial chronic pain or sensorimotor disorders, have not
Neuroplasticity of face sensorimotor cortex 139

been thoroughly investigated in animals or humans. They [15] Meier JD, Aflalo TN, Kastner S, Graziano MS. Complex organi-
represent a fruitful research avenue for providing insights zation of human primary motor cortex: a high-resolution fMRI
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Acknowledgements Brain Res 2006;173(1):165—73.
[18] Ehrsson HH, Geyer S, Naito E. Imagery of voluntary movement of
fingers, toes, and tongue activates corresponding body-part-
The authors’ studies noted herein have been supported by specific motor representations. J Neurophysiol 2003;90(5):
grants from the Canadian Institutes of Health Research, the 3304—16.
Canadian Foundation for Innovation and the Ontario Innova- [19] Huang CS, Sirisko MA, Hiraba H, Murray GM, Sessle BJ. Organi-
tion Trust and Ministry of Research and Innovation. B.J.S. is zation of the primate face motor cortex as revealed by
the holder of a Canada Research Chair. Studies by the authors intracortical microstimulation and electrophysiological iden-
cited in this review had been approved by the University of tification of afferent inputs and corticobulbar projections. J
Toronto Animal Care Committee, in accordance with the Neurophysiol 1988;59(3):796—818.
Canadian Council on Animal Care Guidelines and the regula- [20] Huang CS, Hiraba H, Murray GM, Sessle BJ. Topographical
distribution and functional properties of cortically induced
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