- Email: [email protected]
Neuroplasticity of face primary motor cortex control of orofacial movements
archives of oral biology 52 (2007) 334–337
available at www.sciencedirect.com
journal homepage: www.intl.elsevierhealth.com/journals/arob
Neuroplasticity of face primary motor cortex control of orofacial movements B.J. Sessle *, K. Adachi, L. Avivi-Arber, J. Lee, H. Nishiura, D. Yao, K. Yoshino Faculty of Dentistry, University of Toronto, 124 Edward Street, Toronto, Ontario, Canada M5G 1G6
article info
abstract
Article history:
We have carried out a series of studies to address the role of the face primary motor area (MI)
Accepted 2 November 2006
in the cerebral cortex in trained or semi-automatic orofacial motor behaviours and in behavioural adaptations to an altered oral environment. These studies have utilized intra-
Keywords:
cortical microstimulation (ICMS), reversible cold block or single neurone recordings in face
Motor cortex
MI. Our studies in monkeys have revealed that face MI plays a strategic role in elemental and
Orofacial
learned motor behaviours and in certain aspects of chewing and swallowing. Furthermore,
Adaptation
successful training of awake monkeys in a novel tongue-protrusion task is associated with
Neuroplasticity
significant neuroplastic changes in face MI. These findings in monkeys are supported by
Learning
correlated findings in humans which have revealed significantly enhanced corticomotoneuronal excitability when humans learn the novel tongue-protrusion task. Our related ICMS studies in rats reveal that trimming or extraction of the rat’s lower incisors or damage to the rat’s lingual nerve can result in significant changes in the MI representations of the tongue or jaw muscles. These various findings suggest that the face MI is important in orofacial motor skill acquisition and adaptation to an altered occlusion or loss of teeth or lingual sensory function, and that it reflects dynamic and modifiable constructs that are modelled by behaviourally significant experiences and that are critical to learning and adaptive processes. # 2006 Elsevier Ltd. All rights reserved.
1.
Introduction
The primary motor area (MI) in the cerebral cortex has been documented to play critical roles in sensorimotor integration and control as well as in the learning of new motor skills. This article outlines recent evidence, including our own studies in monkeys, humans and rats, pointing to the importance of face MI in semi-automatic movements such as mastication and swallowing as well as trained orofacial motor behaviour and to its propensity for neuroplastic changes in association with the acquisition of orofacial motor skills or with an altered oral environment.
2. Role of face MI in orofacial sensorimotor functions There are several reports of sensory and motor deficits following either damage to the primate MI (e.g. by stroke) or damage to sensory inputs to the cortex (e.g. by nerve injury) (for review, see refs.1–5). These data are consistent with our own experimental findings in awake monkeys of the effects of reversible cold block of face MI (e.g. refs.5,6). Bilateral cold block of face MI (defined by intracortical microstimulation (ICMS); also see below) was found to interfere with the animal’s successful performance of a novel tongue-protrusion task;
* Corresponding author. Tel.: +1 416 979 4910; fax: +1 416 979 4937. E-mail address: [email protected] (B.J. Sessle). 0003–9969/$ – see front matter # 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2006.11.002
archives of oral biology 52 (2007) 334–337
face MI cold block also modified mastication and masticatoryrelated EMG bursts. Furthermore, short-train stimulation (ICMS; 0.2 ms pulses, 333 Hz, 35 ms) of face MI evoked elemental movements such as jaw opening or tongue protrusion, whereas long-train stimulation (ICMS; 0.2 ms pulses, 50 Hz, 3 s) evoked different patterns of swallowing and masticatory-like movements. In addition, consistent with other studies (for review, see refs.5–7), neurones recorded at many of these same intracortical sites defined by ICMS show ingestive-related activity and/or activity related to the trained tongue-protrusion task or to a trained jaw-closing task, and most MI neurones receive orofacial mechanosensory inputs especially from lips, tongue and teeth. These data collectively indicate that face MI is involved in the control not only of elemental and learned orofacial movements but also of semiautomatic movements such as mastication and swallowing, functions that in the past have been largely attributed to brainstem control mechanisms.
3.
Neuroplasticity of face MI
3.1.
Acquisition of orofacial motor skills
The literature on the function of the limb sensorimotor cortex has underscored the neuroplasticity of MI and of the importance of sensory inputs to the sensorimotor cortex in the acquisition of limb motor skills (for review, see refs.1,2,4). This topic has received little attention in orofacial motor skill acquisition, other than clinical or animal behavioural reports suggesting neuroplasticity or progressive return of function of face sensorimotor cortex following cortical damage or manipulations of orofacial sensory inputs (e.g. refs.1,3–5) and recent findings of face MI neuroplasticity following orofacial task training in humans (see below). We have tested for the possible neuroplasticity of face MI (and SI and cortical masticatory area (CMA)/swallow cortex) related to the learning of a novel orofacial motor skill (e.g. ref.5). In 4 monkeys studied to date, we have applied ICMS at approximately 25,000 intracortical sites and defined the functional properties of over 700 neurones. ICMS and neurone recordings were made over a 1–2 month period before, and again after, a 1–2 month period of training on a novel tongueprotrusion task; this task was comparable to that used in our MI cold block experiments (see above). Compared with pretraining data in these animals and data in control untrained animals, there was a significant increase (12%, p < 0.05, x2 test) after training in the proportion of discrete MI efferent zones for tongue protrusion, as revealed by ICMS and an associated significant decrease (22%, p < 0.001) in zones for lateral tongue movement. In addition, the proportion of MI (and SI neurones) showing tongue protrusion-related activity also significantly increased (55%, p < 0.001), as did the proportion of neurones with mechanosensory inputs from the tongue (30% increase). A lack of analogous changes in CMA/swallow cortex suggests that differential expression of task-related neuroplasticity may occur in these three cortical regions. Correlated studies using transcranial magnetic stimulation (TMS) of human face MI have shown that after only 1 h of training in a tongueprotrusion task analogous to that used in our monkey studies,
335
human subjects show a significant increase in the MI tongue representation, a significant decrease in the TMS-evoked thresholds and increase in the amplitude of TMS-evoked tongue motor potentials.8 Thus, face MI neuroplasticity occurs when humans learn a novel orofacial motor behaviour, a finding consistent with our monkey data and with the enhanced limb MI corticomotor excitability associated with limb motor skill acquisition (e.g. refs.1,2,4). The findings suggest that face MI, like limb MI, may be critical in motor skill learning, reflecting dynamic and adaptive events modelled in a use-dependent manner by behaviourally significant experiences. Furthermore, our MI cold block data (see above) indicate that face MI is also critical in the successful performance of an orofacial motor skill once it is learnt.
3.2.
Intraoral alterations
Several studies have reported neuroplasticity occurs in limb MI as well as SI following peripheral sensory or motor nerve lesions or manipulations of sensory inputs in adult subprimates and primates (e.g. for review, see refs.1,2,4). Although much less investigation has been made of face MI following analogous manipulations, several studies have addressed the effects on face MI of deafferentation of the vibrissae (e.g. by infraorbital nerve transection) or altering their afferent input to the cortex or lesioning the facial nerve that provides the motor supply to the vibrissal muscles (e.g. refs.1,2,4,9). Most of these studies have reported a reduction in the vibrissal representation and an expansion of the adjacent forelimb representation in MI, although no significant changes in face MI have been reported specifically after vibrissal deafferentation.9 No studies appear to have provided any detailed information of orofacial deafferentation effects on the jaw and tongue representations in MI, except for recent TMS studies in humans reporting changes in face MI output effects (see ref.10). Also, it has been reported11 that partial trigeminal deafferentation is not associated 16 days later with any significant changes in rabbit CMA or CMA output effects. In view of the very limited data available, we decided to address the question: does face MI neuroplasticity occur in association with changes in the oral environment, such as the loss or alterations of dental or other oral tissues? It is clear that adaptive behaviours occur when the occlusion is modified or lingual nerve damaged, and in some cases maladaptive behaviours may result. Thus, we tested the effects of trimming of the mandibular incisors (to take them out of occlusion with the maxillary incisors) or loss of one incisor (through extraction) or transection of the left lingual nerve on the ICMS-defined parameters of face MI in anaesthetized rats. We found that altering the occlusion of the teeth by trimming both incisors every alternate day over a period of 1 week induced neuroplastic changes in MI of the rat that were reflected in a significant ( p < 0.05, t-test) reduction in the left and right anterior digastric (AD) representation in left face MI (Table 1); a significant AD reduction also occurred in right face MI. Sham trimming was ineffective in inducing these neuroplastic changes. Although the effects of such multiple trimmings were greater than those of a single trimming, a single trimming session 1 day later nonetheless induced a
336
archives of oral biology 52 (2007) 334–337
Table 1 – The number of positive ICMS sites in left face MI of rats from which EMG activity could be evoked in jaw and tongue muscles Experimental group
Muscle
Positive ICMS sites (mean S.E.M.)
IT
LAD RAD GG
71.5 9.6 * 62.0 8.1 * 67.9 13.5
IE
LAD RAD GG
145.6 17.6 150.9 20.4 * 100.7 22.3
LT
LAD RAD GG
78.9 15.5 74.4 10.4 * 46.0 11.7 **
Muscles: LAD, left anterior digastric; RAD, right anterior digastric; GG, genioglossus. Experimental groups: IT, incisor trimming (both lower incisors); IE, incisor extraction (lower right); LT, lingual nerve transection (left). *p < 0.05 and **p < 0.01 (t-test), experimental group vs. sham group (experimental group values normalized to sham group values).
significant reduction in the AD representation that was reversible.12 Another form of dental manipulation induces quite different changes in face MI of the rat (see Table 1). Under experimental conditions analogous to the incisor trimming study, we found that extraction of the right lower incisor was associated 1 week later with a significant expansion of the AD representation compared to control animals.13 It is also noteworthy that the changes in face MI are not specific to alterations to the teeth. A significant reduction in both AD and genioglossus (GG) representations in left MI occurred 1 week after partial tongue deafferentation produced by left lingual nerve transection (Table 1). Significant reductions in AD and GG representations also occurred in right face MI.14 However, at 3–4 weeks after the transection, the AD and GG representations were significantly increased. Thus, our findings of the effects of incisor trimming or extraction or lingual nerve transection collectively suggest that the form of the MI plasticity may be linked to the specific type of peripheral manipulation, consistent with the view of Franchi9 derived from studies manipulating vibrissal afferent inputs to cortex. Furthermore, the changes that we documented in face MI after lingual nerve transection (a decrease followed by an increase in AD and GG representations) suggest that another critical factor in MI plasticity is its timing relative to the peripheral manipulation. Other factors contributing to the differences in effects (i.e. increase versus decrease) could conceivably include the presence or not of pain, disturbed sensation or sensorimotor disturbance and further study is needed to unravel their potential contributions. A related matter arising from these considerations is whether the MI changes associated with alterations to the teeth or lingual nerve sensory function are the result of the alteration in the sensory inputs to the sensorimotor cortex that allows the animal to adapt to the modified intraoral state, or whether instead the MI changes are the result of a modified sensorimotor behaviour. Most of the literature (see above) on
MI neuroplasticity and motor control would suggest the former and support the view that MI neuroplasticity reflects dynamic, adaptive constructs that are responsive to changes in the sensory environment and indeed underlies the animal’s ability to learn new motor skills or adapt its motor behaviour as it adjusts to the altered peripheral state. Our studies did not address this issue directly, but findings in earlier studies that changes in MI properties can change within minutes as a new sensorimotor task is being learnt (see refs.6–8), would suggest that the MI neuroplastic changes are crucial for the adaptation and acquisition of new motor skills and behaviour appropriate to the altered sensory environment. The effects of incisor trimming that we documented are especially noteworthy in this respect since the rat uses its lower incisors for feeding, fighting, etc., but because of their continuous eruption, it is necessary that the rat also engages in motor behaviours (gnawing, etc.) that provide for their natural attrition of 1– 2 mm/day to match their daily eruption. It is thus possible that changing the dental occlusion by trimming the lower incisors changed the necessity for the rat to engage in its normal motor behaviour and so, based on the concept of use-dependent plasticity, the jaw motor representation was reduced. When the incisors were allowed to erupt subsequently on their own accord (without any trimming intervention), the jaw motor representation rapidly returned to the control (pre-trimming) levels, suggesting that the animal’s re-engagement in its oral motor behaviours to allow for incisor attrition was linked to the restoration of the MI organizational features. In addition, the incisor trimming may have disturbed the close coordination of jaw and tongue movements, and thus account for the disproportionate changes in AD versus genioglossus representations in MI (see Table 1). Further studies are needed to test if the MI neuroplasticity associated with incisor trimming is indeed reflected in functional changes in the motor activities of jaw muscles relative to tongue muscles during oral motor behaviours, and the timing of these changes relative to those in MI.
4.
Conclusions
These studies underscore the critical role played by the face MI in the control of orofacial movements. Our findings suggest that face MI plays a strategic role not only in elemental and learned motor behaviours but also in certain aspects of chewing and swallowing, and may explain why cortical damage, as in stroke, can impair orofacial sensory and motor functions in humans. We have also documented that MI neuroplasticity, as reflected in changes in ICMS features or neuronal activity patterns, is associated with the learning of a novel orofacial motor task and that it may also occur when alterations are made to the dental occlusion, when teeth are lost or when lingual sensory function is compromised. These findings suggest that the face MI neuroplasticity reflects dynamic, adaptive constructs involved in the animal’s ability to learn new orofacial motor skills or adapt its orofacial motor behaviour as it adjusts to the altered peripheral state. Clearly, elucidating the cortical mechanisms associated with motor skill acquisition and with changes in the oral sensory environment is crucial for understanding how humans learn,
archives of oral biology 52 (2007) 334–337
or re-learn, oral motor behaviours or adapt to an altered oral environment, and for developing even better rehabilitative strategies to exploit these mechanisms in humans suffering from orofacial sensorimotor deficits.
Acknowledgements This research was supported by the Canadian Institutes of Health Research, the Canadian Foundation for Innovation and the Ontario Innovation Trust. BJS is the holder of a Canada Research Chair.
references
1. Sanes JN, Donoghue JP. Plasticity and primary motor cortex. Annu Rev Neurosci 2000;23:393–415. 2. Chen R, Cohen LG, Hallett M. Nervous system reorganization following injury. Neuroscience 2002;111:761– 73. 3. Martin RE, Sessle BJ. The role of the cerebral cortex in swallowing. Dysphagia 1993;8:195–202. 4. Ebner FF, editor. Neural plasticity in adult somatic sensory– motor systems. Boca Raton, FL: CRC Press; 2005. 5. Sessle BJ, Yao D, Nishiura H, Yoshino K, Lee JC, Martin RE, et al. Properties and plasticity of the primate somatosensory and motor cortex related to orofacial sensorimotor function. Clin Exp Pharmacol Physiol 2005;32:109–14.
337
6. Yamamura K, Narita N, Yao D, Martin RE, Masuda Y, Sessle BJ. Effects of reversible bilateral inactivation of face primary motor cortex on mastication and swallowing. Brain Res 2002;944:40–55. 7. Yao D, Yamamura K, Narita N, Martin RE, Murray GM, Sessle BJ. Neuronal activity patterns in primate primary motor cortex related to trained or semiautomatic jaw and tongue movements. J Neurophysiol 2002;87:2531–41. 8. Svensson P, Romaniello A, Wang K, Arendt-Nielsen L, Sessle BJ. One hour of tongue-task training is associated with plasticity in corticomotor control of the human tongue musculature. Exp Brain Res 2006;173:165–73. 9. Franchi G. Persistence of vibrissal motor representation following vibrissal pad deafferentation in adult rats. Exp Brain Res 2001;137:180–9. 10. Halkjaer L, Melsen B, McMillan AS, Svensson P. Influence of sensory deprivation and perturbation of trigeminal afferent fibers on corticomotor control of human tongue musculature. Exp Brain Res 2006;170:199–205. 11. Masuda Y, Tachibana Y, Inoue T, Iwata K, Morimoto T. Influence of oro-facial sensory input on the output of the cortical masticatory area in the anaesthetized rabbit. Exp Brain Res 2002;146:501–10. 12. Lee J, Avivi-Arber L, Adachi K, Yao D, Sessle BJ. Motor cortex (MI) neuroplasticity associated with single or multiple trimmings of the rat incisors. Soc Neurosci Abstr 2005:174.1. 13. Avivi-Arber L, Lee J, Sessle BJ. Motor cortex (MI) neuroplasticity may result from extraction of rat mandibular incisor. Soc Neurosci Abstr 2005:174.2. 14. Adachi K, Lee J, Yao D, Sessle BJ. Motor cortex neuroplasticity associated with lingual nerve manipulation in rats. Soc Neurosci Abstr 2004:992.12.
available at www.sciencedirect.com
journal homepage: www.intl.elsevierhealth.com/journals/arob
Neuroplasticity of face primary motor cortex control of orofacial movements B.J. Sessle *, K. Adachi, L. Avivi-Arber, J. Lee, H. Nishiura, D. Yao, K. Yoshino Faculty of Dentistry, University of Toronto, 124 Edward Street, Toronto, Ontario, Canada M5G 1G6
article info
abstract
Article history:
We have carried out a series of studies to address the role of the face primary motor area (MI)
Accepted 2 November 2006
in the cerebral cortex in trained or semi-automatic orofacial motor behaviours and in behavioural adaptations to an altered oral environment. These studies have utilized intra-
Keywords:
cortical microstimulation (ICMS), reversible cold block or single neurone recordings in face
Motor cortex
MI. Our studies in monkeys have revealed that face MI plays a strategic role in elemental and
Orofacial
learned motor behaviours and in certain aspects of chewing and swallowing. Furthermore,
Adaptation
successful training of awake monkeys in a novel tongue-protrusion task is associated with
Neuroplasticity
significant neuroplastic changes in face MI. These findings in monkeys are supported by
Learning
correlated findings in humans which have revealed significantly enhanced corticomotoneuronal excitability when humans learn the novel tongue-protrusion task. Our related ICMS studies in rats reveal that trimming or extraction of the rat’s lower incisors or damage to the rat’s lingual nerve can result in significant changes in the MI representations of the tongue or jaw muscles. These various findings suggest that the face MI is important in orofacial motor skill acquisition and adaptation to an altered occlusion or loss of teeth or lingual sensory function, and that it reflects dynamic and modifiable constructs that are modelled by behaviourally significant experiences and that are critical to learning and adaptive processes. # 2006 Elsevier Ltd. All rights reserved.
1.
Introduction
The primary motor area (MI) in the cerebral cortex has been documented to play critical roles in sensorimotor integration and control as well as in the learning of new motor skills. This article outlines recent evidence, including our own studies in monkeys, humans and rats, pointing to the importance of face MI in semi-automatic movements such as mastication and swallowing as well as trained orofacial motor behaviour and to its propensity for neuroplastic changes in association with the acquisition of orofacial motor skills or with an altered oral environment.
2. Role of face MI in orofacial sensorimotor functions There are several reports of sensory and motor deficits following either damage to the primate MI (e.g. by stroke) or damage to sensory inputs to the cortex (e.g. by nerve injury) (for review, see refs.1–5). These data are consistent with our own experimental findings in awake monkeys of the effects of reversible cold block of face MI (e.g. refs.5,6). Bilateral cold block of face MI (defined by intracortical microstimulation (ICMS); also see below) was found to interfere with the animal’s successful performance of a novel tongue-protrusion task;
* Corresponding author. Tel.: +1 416 979 4910; fax: +1 416 979 4937. E-mail address: [email protected] (B.J. Sessle). 0003–9969/$ – see front matter # 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2006.11.002
archives of oral biology 52 (2007) 334–337
face MI cold block also modified mastication and masticatoryrelated EMG bursts. Furthermore, short-train stimulation (ICMS; 0.2 ms pulses, 333 Hz, 35 ms) of face MI evoked elemental movements such as jaw opening or tongue protrusion, whereas long-train stimulation (ICMS; 0.2 ms pulses, 50 Hz, 3 s) evoked different patterns of swallowing and masticatory-like movements. In addition, consistent with other studies (for review, see refs.5–7), neurones recorded at many of these same intracortical sites defined by ICMS show ingestive-related activity and/or activity related to the trained tongue-protrusion task or to a trained jaw-closing task, and most MI neurones receive orofacial mechanosensory inputs especially from lips, tongue and teeth. These data collectively indicate that face MI is involved in the control not only of elemental and learned orofacial movements but also of semiautomatic movements such as mastication and swallowing, functions that in the past have been largely attributed to brainstem control mechanisms.
3.
Neuroplasticity of face MI
3.1.
Acquisition of orofacial motor skills
The literature on the function of the limb sensorimotor cortex has underscored the neuroplasticity of MI and of the importance of sensory inputs to the sensorimotor cortex in the acquisition of limb motor skills (for review, see refs.1,2,4). This topic has received little attention in orofacial motor skill acquisition, other than clinical or animal behavioural reports suggesting neuroplasticity or progressive return of function of face sensorimotor cortex following cortical damage or manipulations of orofacial sensory inputs (e.g. refs.1,3–5) and recent findings of face MI neuroplasticity following orofacial task training in humans (see below). We have tested for the possible neuroplasticity of face MI (and SI and cortical masticatory area (CMA)/swallow cortex) related to the learning of a novel orofacial motor skill (e.g. ref.5). In 4 monkeys studied to date, we have applied ICMS at approximately 25,000 intracortical sites and defined the functional properties of over 700 neurones. ICMS and neurone recordings were made over a 1–2 month period before, and again after, a 1–2 month period of training on a novel tongueprotrusion task; this task was comparable to that used in our MI cold block experiments (see above). Compared with pretraining data in these animals and data in control untrained animals, there was a significant increase (12%, p < 0.05, x2 test) after training in the proportion of discrete MI efferent zones for tongue protrusion, as revealed by ICMS and an associated significant decrease (22%, p < 0.001) in zones for lateral tongue movement. In addition, the proportion of MI (and SI neurones) showing tongue protrusion-related activity also significantly increased (55%, p < 0.001), as did the proportion of neurones with mechanosensory inputs from the tongue (30% increase). A lack of analogous changes in CMA/swallow cortex suggests that differential expression of task-related neuroplasticity may occur in these three cortical regions. Correlated studies using transcranial magnetic stimulation (TMS) of human face MI have shown that after only 1 h of training in a tongueprotrusion task analogous to that used in our monkey studies,
335
human subjects show a significant increase in the MI tongue representation, a significant decrease in the TMS-evoked thresholds and increase in the amplitude of TMS-evoked tongue motor potentials.8 Thus, face MI neuroplasticity occurs when humans learn a novel orofacial motor behaviour, a finding consistent with our monkey data and with the enhanced limb MI corticomotor excitability associated with limb motor skill acquisition (e.g. refs.1,2,4). The findings suggest that face MI, like limb MI, may be critical in motor skill learning, reflecting dynamic and adaptive events modelled in a use-dependent manner by behaviourally significant experiences. Furthermore, our MI cold block data (see above) indicate that face MI is also critical in the successful performance of an orofacial motor skill once it is learnt.
3.2.
Intraoral alterations
Several studies have reported neuroplasticity occurs in limb MI as well as SI following peripheral sensory or motor nerve lesions or manipulations of sensory inputs in adult subprimates and primates (e.g. for review, see refs.1,2,4). Although much less investigation has been made of face MI following analogous manipulations, several studies have addressed the effects on face MI of deafferentation of the vibrissae (e.g. by infraorbital nerve transection) or altering their afferent input to the cortex or lesioning the facial nerve that provides the motor supply to the vibrissal muscles (e.g. refs.1,2,4,9). Most of these studies have reported a reduction in the vibrissal representation and an expansion of the adjacent forelimb representation in MI, although no significant changes in face MI have been reported specifically after vibrissal deafferentation.9 No studies appear to have provided any detailed information of orofacial deafferentation effects on the jaw and tongue representations in MI, except for recent TMS studies in humans reporting changes in face MI output effects (see ref.10). Also, it has been reported11 that partial trigeminal deafferentation is not associated 16 days later with any significant changes in rabbit CMA or CMA output effects. In view of the very limited data available, we decided to address the question: does face MI neuroplasticity occur in association with changes in the oral environment, such as the loss or alterations of dental or other oral tissues? It is clear that adaptive behaviours occur when the occlusion is modified or lingual nerve damaged, and in some cases maladaptive behaviours may result. Thus, we tested the effects of trimming of the mandibular incisors (to take them out of occlusion with the maxillary incisors) or loss of one incisor (through extraction) or transection of the left lingual nerve on the ICMS-defined parameters of face MI in anaesthetized rats. We found that altering the occlusion of the teeth by trimming both incisors every alternate day over a period of 1 week induced neuroplastic changes in MI of the rat that were reflected in a significant ( p < 0.05, t-test) reduction in the left and right anterior digastric (AD) representation in left face MI (Table 1); a significant AD reduction also occurred in right face MI. Sham trimming was ineffective in inducing these neuroplastic changes. Although the effects of such multiple trimmings were greater than those of a single trimming, a single trimming session 1 day later nonetheless induced a
336
archives of oral biology 52 (2007) 334–337
Table 1 – The number of positive ICMS sites in left face MI of rats from which EMG activity could be evoked in jaw and tongue muscles Experimental group
Muscle
Positive ICMS sites (mean S.E.M.)
IT
LAD RAD GG
71.5 9.6 * 62.0 8.1 * 67.9 13.5
IE
LAD RAD GG
145.6 17.6 150.9 20.4 * 100.7 22.3
LT
LAD RAD GG
78.9 15.5 74.4 10.4 * 46.0 11.7 **
Muscles: LAD, left anterior digastric; RAD, right anterior digastric; GG, genioglossus. Experimental groups: IT, incisor trimming (both lower incisors); IE, incisor extraction (lower right); LT, lingual nerve transection (left). *p < 0.05 and **p < 0.01 (t-test), experimental group vs. sham group (experimental group values normalized to sham group values).
significant reduction in the AD representation that was reversible.12 Another form of dental manipulation induces quite different changes in face MI of the rat (see Table 1). Under experimental conditions analogous to the incisor trimming study, we found that extraction of the right lower incisor was associated 1 week later with a significant expansion of the AD representation compared to control animals.13 It is also noteworthy that the changes in face MI are not specific to alterations to the teeth. A significant reduction in both AD and genioglossus (GG) representations in left MI occurred 1 week after partial tongue deafferentation produced by left lingual nerve transection (Table 1). Significant reductions in AD and GG representations also occurred in right face MI.14 However, at 3–4 weeks after the transection, the AD and GG representations were significantly increased. Thus, our findings of the effects of incisor trimming or extraction or lingual nerve transection collectively suggest that the form of the MI plasticity may be linked to the specific type of peripheral manipulation, consistent with the view of Franchi9 derived from studies manipulating vibrissal afferent inputs to cortex. Furthermore, the changes that we documented in face MI after lingual nerve transection (a decrease followed by an increase in AD and GG representations) suggest that another critical factor in MI plasticity is its timing relative to the peripheral manipulation. Other factors contributing to the differences in effects (i.e. increase versus decrease) could conceivably include the presence or not of pain, disturbed sensation or sensorimotor disturbance and further study is needed to unravel their potential contributions. A related matter arising from these considerations is whether the MI changes associated with alterations to the teeth or lingual nerve sensory function are the result of the alteration in the sensory inputs to the sensorimotor cortex that allows the animal to adapt to the modified intraoral state, or whether instead the MI changes are the result of a modified sensorimotor behaviour. Most of the literature (see above) on
MI neuroplasticity and motor control would suggest the former and support the view that MI neuroplasticity reflects dynamic, adaptive constructs that are responsive to changes in the sensory environment and indeed underlies the animal’s ability to learn new motor skills or adapt its motor behaviour as it adjusts to the altered peripheral state. Our studies did not address this issue directly, but findings in earlier studies that changes in MI properties can change within minutes as a new sensorimotor task is being learnt (see refs.6–8), would suggest that the MI neuroplastic changes are crucial for the adaptation and acquisition of new motor skills and behaviour appropriate to the altered sensory environment. The effects of incisor trimming that we documented are especially noteworthy in this respect since the rat uses its lower incisors for feeding, fighting, etc., but because of their continuous eruption, it is necessary that the rat also engages in motor behaviours (gnawing, etc.) that provide for their natural attrition of 1– 2 mm/day to match their daily eruption. It is thus possible that changing the dental occlusion by trimming the lower incisors changed the necessity for the rat to engage in its normal motor behaviour and so, based on the concept of use-dependent plasticity, the jaw motor representation was reduced. When the incisors were allowed to erupt subsequently on their own accord (without any trimming intervention), the jaw motor representation rapidly returned to the control (pre-trimming) levels, suggesting that the animal’s re-engagement in its oral motor behaviours to allow for incisor attrition was linked to the restoration of the MI organizational features. In addition, the incisor trimming may have disturbed the close coordination of jaw and tongue movements, and thus account for the disproportionate changes in AD versus genioglossus representations in MI (see Table 1). Further studies are needed to test if the MI neuroplasticity associated with incisor trimming is indeed reflected in functional changes in the motor activities of jaw muscles relative to tongue muscles during oral motor behaviours, and the timing of these changes relative to those in MI.
4.
Conclusions
These studies underscore the critical role played by the face MI in the control of orofacial movements. Our findings suggest that face MI plays a strategic role not only in elemental and learned motor behaviours but also in certain aspects of chewing and swallowing, and may explain why cortical damage, as in stroke, can impair orofacial sensory and motor functions in humans. We have also documented that MI neuroplasticity, as reflected in changes in ICMS features or neuronal activity patterns, is associated with the learning of a novel orofacial motor task and that it may also occur when alterations are made to the dental occlusion, when teeth are lost or when lingual sensory function is compromised. These findings suggest that the face MI neuroplasticity reflects dynamic, adaptive constructs involved in the animal’s ability to learn new orofacial motor skills or adapt its orofacial motor behaviour as it adjusts to the altered peripheral state. Clearly, elucidating the cortical mechanisms associated with motor skill acquisition and with changes in the oral sensory environment is crucial for understanding how humans learn,
archives of oral biology 52 (2007) 334–337
or re-learn, oral motor behaviours or adapt to an altered oral environment, and for developing even better rehabilitative strategies to exploit these mechanisms in humans suffering from orofacial sensorimotor deficits.
Acknowledgements This research was supported by the Canadian Institutes of Health Research, the Canadian Foundation for Innovation and the Ontario Innovation Trust. BJS is the holder of a Canada Research Chair.
references
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