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Head Immobilization can Impair Jaw Function
1 Department of Odontology, Clinical Oral Physiology, Umeå University, S-901 87, Umeå, Sweden, and Centre for Musculoskeletal Research, Gävle University, Sweden; and Correspondence: * corresponding author, per-olof.eriksson{at}odont.umu.se
Findings that jaw-opening/-closing relies on both mandibular and head movements suggest that jaw and neck muscles are jointly activated in jaw function. This study tested the hypothesis that rhythmic jaw activities involve an active repositioning of the head, and that head fixation can impair jaw function. Concomitant mandibular and head-neck movements were recorded during rhythmic jaw activities in 12 healthy adults, with and without fixation of the head. In four participants, the movement recording was combined with simultaneous registration of myoelectric activity in jaw and neck muscles. The results showed neck muscle activity during jaw opening with and without head fixation. Notably, head fixation led to reduced mandibular movements and shorter duration of jaw-opening/-closing cycles. The findings suggest recruitment of neck muscles in jaw activities, and that head fixation can impair jaw function. The results underline the jaw and neck neuromuscular relationship in jaw function.
Key Words: human • head • neck • jaw • movement
Studies in animals and humans have showed a biomechanical and anatomical relationship between the jaw and neck regions, and suggested a strong functional linkage between the jaw-face and cranio-cervical motor systems (Abrahams and Richmond, 1977; Alstermark et al., 1992; Abrahams et al., 1993). Head-neck movements are an integral part of natural jaw activities, with head extension in jaw opening and head flexion in jaw closing (Eriksson et al., 1998, 2000; Zafar et al., 2000b). Thus, "functional jaw movements" are the result of a coordinated activation of jaw as well as neck muscles, leading to simultaneous movements in the temporomandibular, atlanto-occipital, and cervical spine joints (Eriksson et al., 2000). In fact, the head starts to move before or simultaneously with the mandible, both in single (Zafar et al., 2000b) and in rhythmic jaw-opening/-closing tasks (Eriksson et al., 2000). This indicates an activation of neck motoneurons in a feed-forward mode. Detailed studies have also showed that the concomitant mandibular and head-neck movements during jaw-opening/-closing tasks are invariant (Zafar et al., 2002). Based on the results from our previous findings in adults, and on findings of both mandibular and head movements in ultrasonic studies of fetal yawning (Sepulveda and Mangiamarchi, 1995), we have suggested that a functional coupling of the jaw and the neck motor systems in natural jaw function is innate (Eriksson et al., 2000; Zafar et al., 2000b). Previous studies of human mandibular movements, in which head movements have been considered as a source of error, add indirect support for the hypothesis that natural jaw function relies on both mandibular and head movements. Thus, different methods to restrict head motion during the recording of jaw movements have been reported (Wood, 1979; Morimoto et al., 1984; Kazazoglu et al., 1994). The "problem" with unwanted head movements during chewing was also reported in a recent brain-mapping study, where more than 20% of the data were excluded due to head movements (Onozuka et al., 2002). Given that head-neck movements are an integral part of jaw behavior, it seems reasonable to assume that restricted head-neck mobility can impair jaw function. This assumption is supported by recent studies of jaw activities in patients with restricted head-neck mobility due to neck injury (Häggman-Henrikson et al., 2002, 2004; Eriksson et al., 2004). The aim of the present study was to test the hypothesis that rhythmic jaw activities include active head movements and recruitment of neck muscles, and that head fixation can impair jaw function. Specifically, the effect of fixation of the head on rhythmic jaw activities was studied in 12 healthy participants by means of an optoelectronic movement-recording technique (Häggman-Henrikson et al., 1998; Zafar et al., 2000a). In four participants, the movement analysis was combined with simultaneous recording of myoelectric activity from jaw and neck/shoulder muscles.
Participants and General Procedure Seven males and five females (ages, 22–37 yrs; mean age, 29 yrs) participated in the study. All participants were free from pain and dysfunction in the jaw and neck regions, and were unaware of the underlying aim of the investigation. They had given their informed consent according to the World Medical Associationhs Declaration of Helsinki. The investigation was approved by the Ethics Committee, Umeå University. Each participant was studied in 2 consecutive sessions, 1 with free and 1 with restricted head-neck movements. For each session, 3 standardized rhythmic jaw motor tasks were performed: (i) self-paced continuous maximal jaw-opening/-closing movements, (ii) paced continuous maximal jaw-opening/-closing movements (in time with a metronome set at 50 beats/min), and (iii) unilateral chewing of 3 pieces of pre-softened chewing gum (weight, 3 g) on the side chosen by the participant. Prior to the start of each recording, the participant was instructed to position the teeth in light contact in the intercuspal position, and this position was used as a reference. Each recording started with a five-second rest period. Each motor task was recorded twice, with an interval of 2 min between recordings. In the first session, the participants were seated comfortably in an upright position in an armchair with back support up to the mid-scapular level, but without a headrest, allowing for free unrestricted head-neck movements. In the second recording session, the head-neck was immobilized by means of an adjustable head fixation frame attached to the chair. The fixation frame was individually adjusted to the participant’s head while he/she was sitting in a relaxed unrestricted upright position. Thereafter, the frame was adjusted to the size and position of the participant’s head, and fixated firmly with screw-retained pads without provoking pain. Movements of the mandible and the head were simultaneously monitored in 3 dimensions (3-D), by means of a wireless optoelectronic recording system with a sampling rate of 50 Hz (MacReflex®, Gothenburg, Sweden) (Josefsson et al., 1996).
The set-up allowed movements to be accurately recorded with a spatial resolution of 0.02 mm within a working volume of 45 x 55 x 50 cm. Spherical low-weight retro-reflective markers (5 mm in diameter) were attached to the mandible and to the head (Fig. 1
Analysis By means of co-ordinate transformation, the changes in 3-D position of the mandibular markers were adjusted for the changes in 3-D position of the head markers. This mathematical 3-D compensation for head movement allowed for segmental analysis of the isolated mandibular movements in relation to the head (Zafar et al., 2000a). The mandibular and the head movement amplitudes were expressed as 3-D trajectories, calculated according to the formula:
where s and p indicate start and peak positions. All movement estimates were based on the data from 10 movement cycles, 5 consecutive cycles from each test.
Electromyography
Statistics
No differences were found between the 2 repeated tests for any of the parameters. Therefore, the data from the 2 tests in each recording session were pooled, and mean values were calculated for each participant.
Movement Amplitudes and Cycle Times
Muscle Activity Even with head fixation, activity in neck muscles was seen during jaw opening (Fig. 3  ), and this was a general finding for the maximal jaw-opening/-closing tasks (Figs. 4a, 4b). For jaw closing, only sternocleidomastoid muscle activity was seen, during chewing in 58% of the cycles without head fixation, and in 80% of cycles with head fixation (Figs. 4c, 4d).
This study tested the hypothesis that concomitant head-neck movements in natural jaw-opening/-closing tasks are due to an active repositioning of the head. The results showed that complete immobilization of the head during jaw activities was virtually impossible. Despite efforts to fixate the head-neck, synchronized head movements were seen. Furthermore, neck muscle activity was recorded during jaw-opening both with and without head fixation. These findings suggest the presence of a neuronal circuitry for active head movements during jaw activities, and that head-neck movements are an integral part of natural jaw function. Moreover, our experimental restriction of head movements implies that reduced head-neck mobility can impair jaw function. The choice of technique for the recording of myoelectric activity in jaw muscles relates to the question to be answered. Thus, whereas surface electrodes are usually selected if one wishes to gain information on global jaw muscle activity (Møller, 1966), detailed analysis of the recruitment order of separate muscular regions and single motor units requires other techniques (Eriksson et al., 1984; Stålberg and Eriksson, 1987). For the purpose of this study, to estimate the "on-off" state of jaw and neck muscle activity during jaw-opening/-closing tasks, without intending to analyze the order of recruitment of muscles or specific regions of muscles, we used surface electrodes with fixed interelectrode distances. The finding of myoelectric activity in both the sternocleidomastoid and the trapezius muscles in the jaw-opening phase, indicating that these muscles were recruited simultaneously with the jaw-opening muscles, agrees with previous findings (Eriksson et al., 1998). The sternocleidomastoid muscle activity also in the closing phase during chewing may reflect a stabilizing role of this muscle in head-neck movements involved in jaw activities. The head movements seen, despite firm fixation of the head, were probably enabled by soft-tissue movement under the fixation pads, allowing for small movements within the frame. This finding in itself gives indirect support for an active head repositioning during jaw activities. An active repositioning of the head is also suggested by our finding of neck muscle activity even with the head fixed. Motor performance can be evaluated by amplitude, speed, acceleration, jerkiness, force, coordination, direction, and endurance of movements. In the present study, we tested the hypothesis that restriction of movements in the atlanto-occipital joint and cervical spine joints, which are simultaneously involved in natural jaw actions, can impair jaw function. Notably, with head fixation, the mandibular movement amplitudes were reduced by more than 20% for the self-paced maximal jaw-opening task, and for this task the jaw-opening/-closing cycles were also shorter. There was no significant reduction in mandibular movement for the other tasks during head fixation. This result is in line with previous findings of a proportional involvement of the neck system in jaw function, with larger head movements in maximal jaw-opening compared with tasks with small mandibular movements, such as chewing of a small soft bolus (Eriksson et al., 2000; Häggman-Henrikson and Eriksson, 2004). Mandibular movements in chewing are governed by central neural networks, located in the brainstem, termed the "central pattern generator" (CPG). In the executed mandibular movements, extero- and proprioceptive peripheral input interacts with these central programs (Lund, 1991; Nakamura and Katakura, 1995; Lund et al., 1998). Previous findings of concomitant mandibular and head-neck movements, in both single (Zafar et al., 2000a) and rhythmic (Eriksson et al., 2000) jaw-opening/-closing activities, have led us to propose that natural jaw function is based on integrated activity of both cranial and cervical motoneurons, with neural commands in common to recruit, jointly, mandibular and neck muscles in a coordinated and pre-programmed mode. Recent evidence showing that head-neck movement amplitudes during chewing are affected by texture and size of bolus indicates influence from feedback systems on central neural networks, controlling posture and movements of the head-neck during jaw function (Häggman-Henrikson and Eriksson, 2004). From our previous and present findings, we suggest that central neural networks underlying natural jaw activities are likely to extend caudally in the brainstem, and also include cervical spine segments. Such neural organization would allow for recruitment of jaw and neck muscle synergies and, accordingly, result in concomitant and coordinated mandibular and head-neck movements in natural jaw function. In consequence, an extended approach is suggested for future research in central mechanisms behind jaw motor behavior, thus including head-neck motor control. In fact, recent animal studies, undertaken without and with fixation of the head in a stereotaxic apparatus, seem to have opened this new line of research (Igarashi et al., 2000; Zeredo et al., 2002, 2003). In man, the relationship between the jaw and neck motor systems has recently also been examined by analysis of the effect of experimental neck pain on jaw motor behavior (Komiyama et al., 2005; Svensson et al., 2005). In conclusion, the present results suggest that head movements during jaw activities are due to recruitment of neck muscles, and that immobilization of the head can impair jaw function. The findings support and extend our suggestion, from previous investigations, that head-neck motor control is an integrative part of natural jaw behavior. Analysis of present and previous data therefore suggests an extended approach in research on mechanisms behind jaw motor control.
The skillful technical assistance of Mr. Jan Öberg and the programming assistance of Mr. Mattias Backén are gratefully acknowledged. This work was supported by the Faculty of Medicine, Umeå University, the Swedish Dental Society, the Arnerska Research Fund, and RTP (The Swedish Association of Survivors of Traffic Accidents and Polio). Received for publication July 20, 2005. Revision received June 13, 2006. Accepted for publication July 17, 2006.
Journal of Dental Research, Vol. 85, No. 11,
1001-1005 (2006)
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