Do Longus Capitis and Colli Really Stabilise the Cervical Spine? a Study of Their Fascicular Anatomy and Peak Force Capabilities

Do longus capitis and colli really stabilise the cervical spine? A study of their fascicular anatomy and peak force capabilities

Original article

Ewan Kennedy1 BPhty, PhD Michael Albert2 PhD Helen Nicholson3 MD

1 School of Physiotherapy, University of Otago, Dunedin 9016, New Zealand 2 Department of Computer Science, University of Otago, Dunedin 9016, New Zealand 3 Department of Anatomy, University of Otago, Dunedin 9016, New Zealand

Correspondence to: Ewan Kennedy, School of Physiotherapy, University of Otago, Dunedin, New Zealand. Phone: +643 479 5424. Email: [email protected]

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Ethical approval for each stage of this research was sought and received from the University of Otago and Lower South Regional Health and Disability Ethics Committees, Dunedin, New Zealand. Conflicts of interest: none.

ABSTRACT

Background

Longus capitis and colli are proposed to play a role in stabilising the cervical spine, targeted in clinical and research practice with cranio-cervical flexion. However, it is not clear if these muscles are anatomically or biomechanically suited to a stabilising role.

Objectives

To describe the fascicular morphology of the longus capitis and colli, and estimate their peak force generating capabilities across the individual cervical motion segments.

Study Design

Biomechanical force modelling based on anatomical data

Methods

Three-part design including cadaveric dissection (n=7), in vivo MRI muscle volume calculation from serial slices in young healthy volunteers (n=6), and biomechanical modelling of the peak force generating capacities based on computed tomography scans of the head and neck.

Results

Longus capitis and colli are small muscles spanning multiple cervical motion segments. Bilateral peak flexion torque estimates were higher in the upper cervical spine (0.5 Nm), and unlikely to affect motion below the level of C5 (<0.2 Nm). Peak shear estimates were negligible (<20 N), while peak compression estimates were small (<80 N).

Conclusions

These data highlight the complex anatomy and small force capacity of longus capitis and colli, and have implications for their function. In particular, the small peak compression forces indicate that these muscles have a limited capacity to contribute to cervical stability via traditional mechanisms. This implies that the mechanism(s) by which cranio-cervical flexion exercises produce clinical benefits is worth exploring further.

Key words: neck muscles; anatomy; neck pain; biomechanics; longus capitis; longus colli

Do longus capitis and colli really stabilise the cervical spine? A study of their fascicular anatomy and peak force capabilities

INTRODUCTION

The longus capitis and colli are two muscles located deep in the anterior neck, lying against the cervical spine. These muscles are often termed the ‘deep cervical flexors’, and are proposed to play a role in stabilising the cervical spine (Falla et al., 2004). Dysfunction of these muscles has been shown in whiplash (Jull et al., 2004) and chronic neck pain (Falla et al., 2004), utilising the cranio-cervical flexion test (CCFT) (Jull et al., 2008b). Briefly, in these conditions the longus muscles are shown to have reduced activity, coupled with an increase in sternocleidomastoid activity (Falla, 2004, Falla et al., 2004). Furthermore, these findings have led to the development of targeted rehabilitation exercises (Jull et al., 2008a, Jull et al.,

2002, Jull et al., 2009). In contrast to these clinical advances, the biomechanical ability of the longus muscles to contribute to cervical motion or generate stability has received little attention. Given that clinical advances are based on the anatomical contribution of longus capitis and colli, a closer look at the fascicular anatomy and functional capabilities of these muscles is warranted.

Longus capitis is described as running from the basilar portion of the occiput to the anterior tubercles on the transverse processes of C3-C6 (Moore et al., 2014, Sinnatamby, 2011,

Standring et al., 2016, Testut, 1899). Longus colli is usually described in three portions: a vertical portion running from the anterior vertebral bodies of C2-4 to the anterior vertebral bodies of C5-T3; a superior oblique portion running from the anterior tubercle of the atlas to the anterior tubercles on the transverse processes of C3-C5; and an inferior oblique portion

3 running from the anterior tubercles on the transverse processes of C5 and C6 to the vertebral bodies of T1-T3 (Sinnatamby, 2011, Standring et al., 2016, Testut, 1899). However, the relative size and importance of these parts of longus colli is unclear. More detailed anatomical research supports this fascicular arrangement of longus capitis and provides morphological data, but gives little further insight into longus colli (Kamibayashi and

Richmond, 1998). Histologically, the longus muscles have been shown to have a mixed type I and II fibre composition (Cornwall and Kennedy, 2015, Miller et al., 2016), that is in contrast to predominantly type I fibres in cervical multifidus (Boyd-Clark et al., 2001).

The functional abilities of longus capitis and colli are far less agreed upon. Anatomical texts state that longus capitis flexes the head, while longus colli flexes the neck (Sinnatamby,

2011, Standring et al., 2016, Testut, 1899). Some descriptions go further, indicating that the longus muscles produce lateral flexion and contralateral rotation (Moore et al., 2014,

Standring et al., 2016). These statements appear speculative rather than based on formal investigation and, given their small size, potentially overstate the functional abilities of the longus muscles. In more detailed research, Vasavada et al (1998) estimates that in the neutral position the longus muscles could contribute to 17% of the total flexion moment generating capacity, but would not contribute substantially to any other movements. This contrasts with the anatomical descriptions. How this flexion force might affect the individual motion segments is not clear. Fundamental electromyographic (EMG) studies of longus colli function indicate it is inactive at rest, and most active during voluntary movements

(Fountain et al., 1966, Vitti et al., 1973), findings which are generally supported by more modern methods (Conley et al., 1995, Falla et al., 2003).

Clinical literature offers a different functional perspective, commonly referring to the longus muscles as ‘stabilisers’ of the cervical spine (Beer et al., 2012, Falla et al., 2004, Jull et al.,

2004). However, evidence to support this view is lacking. A key paper cited in support of this stabilising role concludes: “… perhaps the most fundamental conclusion of our study is that the internal paraspinal musculature is very important during voluntary movements; in fact, the large, multilink superficial muscles with larger moment arms may be the more effective

‘‘stabilisers” (Winters and Peles, 1990 pg. 477). Another reports only correlation (between longus colli cross-sectional area and cervical curvature), but clearly implies causation

(Mayoux-Benhamou et al., 1994). Given the potential importance of these muscles in a range of clinical neck disorders, and such contrasting views of their functional role, a greater understanding of their basic capabilities is needed. This would inform clinicians and researchers alike when considering the function of these muscles, and their potential contribution to clinical disorders. With this in mind, the purpose of this research is to describe the fascicular morphology of the longus capitis and colli, and estimate their peak force generating capabilities across the individual cervical motion segments.

METHODS

The materials and methods of this research have been published previously with reference to the sternocleidomastoid muscle (XX). This study utilises the same methods for the longus capitis and colli muscles. The following summarises the methods involved. This research involved three parts: dissection to reveal the architecture and morphology of longus capitis and colli; magnetic resonance imaging (MRI) of these muscles in healthy volunteers to measure in vivo muscle volumes; and biomechanical modelling of muscle peak force generating capacities across the individual cervical motion segments.

Dissection

The longus capitis and colli muscles were examined in seven embalmed cadavers (three males age 65-95, four females age 63-93) with ethical approval received from the University

XX. Access to the muscles was gained by blunt separation of the spine from the soft tissues of the throat, leaving the prevertebral fascia intact. When this layer was clearly identified the skull was sectioned in the coronal plane to gain access to their superior extent and attachment sites. Fascicles were identified based on unique attachment sites, and morphological data recorded for each. Length was measured to the nearest millimetre with tendinous tissue (termed ‘muscle length’ and without (termed ‘fascicle length’) tendinous tissue using a metal ruler. Volume was measured to the nearest millilitre using water displacement in a measuring cylinder. Where both sides of a cadaver were dissected mean values were calculated to represent that cadaver. Physiological cross-sectional area was calculated using the equation: PCSA = Volume / Fascicular length.

Magnetic resonance imaging

Magnetic resonance imaging was performed on six young, healthy volunteers (three males age 24-37, three females age 26-28). Ethical approval was granted by the XX regional Ethics

Committee (LRS/07/04/011), each volunteer gave informed consent, and their rights were respected. The scans utilised a Philips Acheiva 1.X T machine using a neurovascular coil. The main images were three blocks of axial T1-weighted scans; each 32 slices, 3 mm thick with 0 mm gap, field of view 410mm, TR 500ms, TE 13ms, matrix 480 x 512, 4 number of signals averaged (NSA). Muscle volumes were calculated using the Cavalieri method, a well- established stereological method for calculating volumes from slices (Roberts et al., 1993).

Tracing was completed using OsiriX software (www.osirix-viewer.com). The accuracy of these measurements were validated against an object of known area and volume scanned in a weekly quality assurance test, and assessed using a paired t-test and analysis of differences. Reproducibility was checked by repeating the measurements in a randomly selected subject and analysed using an intra-class coefficient (ICC).

Biomechanical modelling

Force modelling of the longus muscles were developed using five sets of computed tomography (CT) scans from oncology archives at a tertiary hospital (four males mean age

50 years, one female 57 years). Further ethical approval was granted for this part of the study by the XX regional Ethics Committee (LRS/06/09/037). The force modelling involved plotting three-dimensional coordinates for muscle attachments, instantaneous axes of rotation (IARs), and vertebral tilt angles using OsiriX software. These coordinates and angles were then used to calculate the peak torque, compression and shear force generated by each fascicle across the cervical motion segments.

The positions of the IARs were plotted from C2/3 to C6/7 based on the previous work of

Amevo et al (Amevo et al., 1991a, Amevo et al., 1991b, c). Note as IARs were not available for the atlanto-occipital or atlanto-axial joints the peak force capacity of longus capitis at these levels were not calculated. Muscle volumes obtained from healthy young volunteers in the MRI study were incorporated into the model by recalculating the dissection-derived

PCSA values, substituting MRI muscle volumes into the equation (PCSA = Fascicle volume /

Fascicle length). Fascicular length values were taken from the dissection study, as there was no reliable way of determining fascicle length (excluding tendinous tissue) in vivo from the

MR images. These data were used to estimate PCSA values for young, healthy males and females, and entered into the biomechanical modeling spreadsheets to produce force estimates. As the fascicular arrangement of longus colli was variable, modelling of longus colli was based on the fascicles identified in at least half the cadavers examined.

Calculations

Force estimates were calculated based on the equation:

Peak force = PCSA x Specific tension (K)

The specific tension is a constant that reflects the relationship between muscle PCSA and peak force capacity, and is a source of some debate. To acknowledge this, and in line with previous work (Bogduk et al., 1992), the tabled results are presented as an expression of specific tension to allow readers to substitute alternative specific tension values, should they wish to. Each force is calculated for a single muscle, and can be doubled for bilateral muscle actions.

Shear and compression Anterior – posterior shear and vertical compression were derived from the orientation of the fascicle in the sagittal plane. Shear and compression represent the two perpendicular vector components of the sagittal force produced by each fascicle. Values were obtained by calculating the sagittal (y and z) components of the force produced by each fascicle with reference to the tilt of each vertebral level, as described by Bogduk et al (1992).

A fascicle's unit direction vector was computed by taking the difference of the x, y and z coordinates at each of its attachment sites, and then dividing by the length of the fascicle

(obtained by the Pythagorean Theorem). The magnitude of these forces was then computed by projecting the muscle unit vector, multiplied by the peak force values in each of these directions. Without a specific tension at this point in the calculation, the peak force was represented by the PCSA value.

Torque Torque was calculated as the force capacity in the sagittal plane multiplied by the length of the moment vector (MV). The moment vector is simply the line from the IAR of the vertebrae to the fascicle, which meets it at right angles. The force capacity in the sagittal plane is obtained by multiplying the peak force of the muscle (using the PCSA value) by the length of its projection to the sagittal plane divided by its total length.

RESULTS

Dissection

The longus muscles lie closely against the anterolateral aspect of the cervical spine, running longitudinally (Figure 1). Both muscles had complex architecture with multiple attachment sites broadly consistent with descriptions in anatomical texts. Morphological data for each are presented in Tables 1 and 2.

The longus capitis had a consistent arrangement from the basi-occiput superiorly, to the anterior tubercles of C3, 4, 5 and 6. Complicating this arrangement was an aponeurosis on the anterior surface of the muscle, which fused the more superficial fascicles (to C5 and C6) together in the middle as shown in Figure 2. This feature was consistent, and has been noted previously (Kamibayashi and Richmond, 1998). This created a muscle belly superior to the aponeurosis, and slips inferior to the aponeurosis attaching to C5 and C6. Small fascicles reaching further down to T2 and T3 were identified in two cadavers, and to the atlanto-axial joint capsule in one cadaver.

Longus colli included superior oblique, vertical and inferior oblique portions based on unique attachment sites, consistent with previous descriptions. Individual fascicles were small and composed of mixed muscle and tendinous tissue (Figure 3). Morphological data shows the portions were unequal in size: superior oblique > vertical > inferior oblique (Table

2). The inferior oblique was particularly small, at the lower limit of our ability to measure muscle volumes using the methods described. Moreover, there was considerable variation in the individual fascicle arrangement between cadavers (Table 2).

TABLE 1. Fascicular anatomy and morphology of longus capitis

Mean muscle Mean fascicle Mean volume n length (cm) length (cm) (ml) Mean PCSA (cm²) Males (n=3) Superior belly 3 - 3.93 (0.33) 1.21 (0.40) 0.31 (0.12) AA joint 0 - - - - C3 3 6.63 (0.26) 5.29 (0.59) 0.75 (0.00) 0.15 (0.01) C4 3 8.97 (0.40) 6.34 (1.51) 0.79 (0.26) 0.12 (0.01) C5 3 11.22 (0.28) 4.23 (0.96) 0.42 (0.14) 0.10 (0.02) C6 3 12.60 (0.41) 4.96 (1.13) 0.83 (0.26) 0.17 (0.02) T2 1 19.80 10.20 0.50 0.05 T3 1 20.70 6.90 0.25 0.04 Total 3 4.04 (0.59) 0.83 (0.13)

Females (n=4) Superior belly 4 - 3.71 (0.45) 0.93 (0.53) 0.25 (0.14) AA joint 1 4.10 1.90 0.10 0.05 C3 4 5.99 (0.57) 4.03 (0.34) 0.71 (0.36) 0.18 (0.10) C4 4 7.76 (0.61) 6.00 (1.57) 0.60 (0.14) 0.10 (0.03) C5 4 9.51 (1.10) 3.76 (0.45) 0.35 (0.17) 0.09 (0.04) C6 4 11.13 (1.21) 5.36 (1.64) 0.84 (0.79) 0.15 (0.12) T2 1 18.60 8.00 0.40 0.05 T3 1 17.10 9.40 0.50 0.05 Total 4 3.61 (1.57) 0.80 (0.37)

Abbreviations: AA, atlanto-axial Values are presented as mean (standard deviation)

TABLE 2. Fascicular anatomy and morphology of longus colli

Males Females Muscle Fascicle Muscle Fascicle Portion and length length Volume PCSA length length Volume PCSA attachments n (cm) (cm) (ml) (cm²) n (cm) (cm) (ml) (cm²) Superior oblique Occiput C4 1 8.2 2.5 0.1 0.0 0 C1 C3 3 4.0 (0.3) 3.2 (0.4) 0.2 (0.2) 0.1 (0.1) 4 3.6 (0.5) 2.9 (0.5) 0.2 (0.1) 0.1 (0.0) C4 3 5.8 (0.3) 5.1 (0.2) 0.6 (0.2) 0.1 (0.0) 4 5.3 (0.5) 4.2 (0.7) 0.5 (0.2) 0.1 (0.0) C5 2 7.5 (0.4) 4.4 (2.8) 0.3 (0.2) 0.1 (0.0) 2 6.3 (0.7) 4.7 (0.4) 0.2 (0.1) 0.0 (0.0) C6 0 1 7.9 3.6 0.1 0.0 C2 C4 1 3.6 2.9 0.2 0.1 3 3.1 (0.2) 2.7 (0.5) 0.2 (0.1) 0.1 (0.0) C5 3 4.6 (0.7) 4.1 (0.5) 0.4 (0.3) 0.1 (0.1) 4 4.1 (0.3) 3.2 (0.3) 0.3 (0.1) 0.1 (0.0) C6 3 7.1 (1.4) 5.7 (0.9) 0.4 (0.1) 0.1 (0.0) 2 5.5 (0.2) 3.0 (0.6) 0.4 (0.2) 0.1 (0.0) C3 C4 0 1 3.0 3.0 0.1 0.0 C5 0 1 2.7 2.3 0.1 0.0 C6 3 4.5 (1.2) 3.7 (0.9) 0.2 (0.1) 0.1 (0.0) 3 3.9 (0.1) 2.6 (0.3) 0.1 (0.1) 0.1 (0.0) Subtotal 3 2.1 (0.8) 0.5 (0.1) 4 1.5 (0.3) 0.4 (0.1) Vertical C1 T2 0 1 13.7 4.5 0.2 0.0 C2 C6 1 8.0 4.9 0.1 0.0 0 C7 1 10.6 5.1 0.2 0.0 1 8.5 4.2 0.2 0.0 T1 3 10.9 (1.0) 4.9 (0.3) 0.5 (0.3) 0.1 (0.1) 3 10.1 (0.4) 3.8 (1.1) 0.2 (0.1) 0.1 (0.0) T2 3 13.6 (1.9) 7.2 (2.3) 0.5 (0.4) 0.1 (0.1) 4 11.5 (0.8) 4.7 (1.8) 0.3 (0.2) 0.1 (0.0) T3 1 15.9 7.9 0.8 0.1 0 C3 C5 1 4.0 1.9 0.1 0.1 0 C6 0 1 5.3 2.5 0.1 0.0 C7 1 8.6 3.6 0.2 0.0 2 6.3 (0.0) 2.4 (1.3) 0.1 (0.0) 0.0 (0.0) T1 2 8.2 (0.7) 2.0 (0.1) 0.1 (0.0) 0.1 (0.0) 3 7.7 (0.8) 3.3 (1.0) 0.2 (0.1) 0.1 (0.0) T2 0 3 9.5 (1.1) 4.5 (1.1) 0.2 (0.2) 0.1 (0.0) C4 C6 0 1 3.1 2.1 0.1 0.0 C7 0 1 5.1 4.3 0.1 0.0 T1 1 6.6 5.5 0.2 0.0 0 C5 T1 0 1 5.3 2.4 0.1 0.0 C6 T1 1 3.9 2.5 0.1 0.0 1 4.2 3.7 0.1 0.0 Subtotal 3 1.7 (0.1) 0.3 (0.1) 4 1.0 (0.2) 0.3 (0.1) Inferior oblique C5 T1 0 1 5.2 4.3 0.2 0.0 T2 1 9.0 2.9 0.2 0.1 2 7.7 (1.1) 4.8 (1.6) 0.2 (0.0) 0.0 (0.0) C6 T1 2 4.9 (0.8) 3.7 (0.0) 0.2 (0.1) 0.1 (0.0) 2 4.1 (1.1) 3.2 (1.2) 0.1 (0.0) 0.0 (0.0) T2 3 6.1 (0.7) 4.3 (0.7) 0.2 (0.1) 0.1 (0.0) 4 6.2 (0.5) 4.1 (1.3) 0.3 (0.1) 0.0 (0.0) T3 1 8.7 4.8 0.5 0.1 1 6.7 2.8 0.1 0.0 C7 T3 1 6.3 5.7 0.1 0.0 0 Subtotal 3 0.6 (0.2) 0.1 (0.0) 4 0.5 (0.2) 0.1 (0.1) Total 3 4.4 (1.2) 1.0 (0.2) 4 2.9 (0.2) 0.8 (0.1)

Values are presented as mean (standard deviation)

Data underlined represent ‘typical’ fascicles present in at least half the cadavers examined

FIGURE 1. Anterior view of longus capitis and colli. Note the superficial aponeurosis in the mid-section of longus capitis, and the superior muscle belly (*).

FIGURE 2. Lateral view of longus capitis showing the fascicles attaching to the anterior tubercles of C3, C4, C5 and C6 respectively. Note how the fascicles to C5 and C6 fuse at the aponeurosis (*).

FIGURE 3. Anterolateral view of longus colli illustrating fascicles of the superior oblique superiorly detached from the anterior tubercle of C1. Note their small size and mix of muscle and tendinous tissue.

Magnetic resonance imaging

The magnetic resonance images showed the longus muscles well. The area measurement accuracy was acceptable, with a mean difference of 0.04 cm2 and 95% limits of agreement from -0.10 to 0.19 cm2. The ICC for reproducibility of muscle volume calculations were 0.993 with a 95% confidence interval of 0.951 – 0.999. Muscle volumes were calculated for males and females (Table 3), and compared to those found in dissection. One female had a relatively large longus colli (8.0 cm2), but otherwise the MRI muscle volumes were consistent.

TABLE 3. Comparison of dissection and MRI muscle volumes

MRI volumes (cm2) Dissection volumes (cm2) Longus Capitis Males 7.3 (0.3) 4.0 (0.6) Females 4.9 (0.3) 3.6 (1.6) Longus Colli Males 7.5 (0.4) 4.4 (1.2) Females 5.7 (2.1) 2.9 (0.2) Values are presented as mean (standard deviation)

Biomechanical modelling

The peak force capabilities of the longus muscles are presented as an expression of specific tension in Tables 4-6. Figures 3-6 present force estimates based on a specific tension of 15

Nm2, a mid-range value for data derived from MRI volumes (Fukunaga et al., 1996). The forces estimated are very modest, particularly for flexion torque. Peak compression force estimates were greatest between the occiput and C4 (Figure 5, Table 5). Shear capacity was minimal (Figure 6, Table 6), emphasised by posterior shear at some levels (for example, occiput – C2) and anterior shear at others.

TABLE 4. Mean peak flexion torque exerted by longus capitis and colli as an expression of specific tension (K)

Cervical level C2/3 C3/4 C4/5 C5/6 C6/7

Longus capitis Males C3 0.0013K (0.0003) C4 0.0013K (0.0004) 0.0015K (0.0005) C5 0.0028K (0.0011) 0.0027K (0.0008) 0.0035K (0.0006) C6 0.0033K (0.0016) 0.0032K (0.0014) 0.0033K (0.0016) 0.0043K (0.0006) Total 0.0087K (0.0013) 0.0074K (0.0012) 0.0068K (0.0012) 0.0043K (0.0006) Females C3 0.0013K (0.0003) C4 0.0008K (0.0002) 0.0009K (0.0003) C5 0.0019K (0.0007) 0.0019K (0.0006) 0.0025K (0.0005) C6 0.0021K (0.0010) 0.0021K (0.0009) 0.0021K (0.0011) 0.0027K (0.0004) Total 0.0061K (0.0008) 0.0049K (0.0008) 0.0046K (0.0008) 0.0027K (0.0004)

Longus colli Males SO 0.0054K (0.0002) 0.0043K (0.0002) 0.0025K (0.0002) 0.0011K (0.0001) Vertical 0.0022K (0.0003) 0.0017K (0.0004) 0.0014K (0.0002) 0.0010K (0.0002) 0.0013K (0.0004) IO 0.0006K (0.0001) Total 0.0077K (0.0004) 0.0060K (0.0003) 0.0040K (0.0002) 0.0021K (0.0002) 0.0018K (0.0004) Females SO 0.0057K (0.0002) 0.0043K (0.0003) 0.0024K (0.0002) 0.0014K (0.0002) Vertical 0.0015K (0.0002) 0.0015K (0.0002) 0.0012K (0.0002) 0.0009K (0.0002) 0.0011K (0.0003) IO 0.0005K (0.0001) Total 0.0073K (0.0005) 0.0058K (0.0003) 0.0036K (0.0003) 0.0023K (0.0003) 0.0015K (0.0003) Abbreviations: SO, Superior oblique; IO, Inferior oblique Values presented are mean (standard deviation)

TABLE 5. Mean peak compression exerted by longus capitis and colli as an expression of specific tension (K)

Cervical level

C0/1 C1/2 C2/3 C3/4 C4/5 C5/6 C6/7 C7/T1 T1/2

Longus capitis Males C3 0.25K (0.01) 0.25K (0.01) 0.25K (0.01) C4 0.22K (0.01) 0.22K (0.00) 0.23K (0.00) 0.23K (0.00) C5 0.42K (0.02) 0.42K (0.01) 0.44K (0.00) 0.44K (0.00) 0.43K (0.01) C6 0.49K (0.03) 0.50K (0.02) 0.53K (0.00) 0.53K (0.00) 0.52K (0.00) 0.51K (0.02) Subtotal 1.38K (0.12) 1.38K (0.12) 1.44K (0.13) 1.19K (0.13) 0.96K (0.05) 0.51K (0.02) Females C3 0.24K (0.01) 0.24K (0.00) 0.24K (0.01) C4 0.13K (0.00) 0.13K (0.00) 0.14K (0.00) 0.14K (0.00) C5 0.29K (0.01) 0.29K (0.01) 0.31K (0.00) 0.31K (0.00) 0.30K (0.01) C6 0.32K (0.02) 0.32K (0.01) 0.34K (0.00) 0.34K (0.00) 0.34K (0.00) 0.33K (0.01) Subtotal 0.98K (0.07) 0.99K (0.07) 1.03K (0.08) 0.78K (0.09) 0.64K (0.02) 0.33K (0.01)

Longus colli Males SO 0.43K (0.04) 0.90K (0.00) 0.89K (0.00) 0.56K (0.00) 0.24K (0.00) Vertical 0.33K (0.00) 0.43K (0.00) 0.44K (0.00) 0.44K (0.00) 0.44K (0.00) 0.43K (0.00) 0.13K (0.00) IO 0.21K (0.00) 0.21K (0.00) 0.10K (0.00) Subtotal 0.43K (0.04) 1.24K (0.04) 1.32K (0.04) 1.00K (0.04) 0.68K (0.04) 0.64K (0.04) 0.64K (0.04) 0.23K (0.02) Females SO 0.41K (0.01) 0.94K (0.00) 0.88K (0.00) 0.54K (0.00) 0.32K (0.00) Vertical 0.24K (0.00) 0.35K (0.00) 0.36K (0.00) 0.36K (0.00) 0.36K (0.00) 0.36K (0.00) 0.14K (0.00) IO 0.18K (0.00) 0.18K (0.00) 0.12K (0.00) Subtotal 0.41K (0.07) 1.18K (0.06) 1.23K (0.06) 0.90K (0.05) 0.68K (0.05) 0.54K (0.03) 0.53K (0.03) 0.26K (0.01)

Abbreviations: SO, Superior oblique; IO, Inferior oblique Values presented are mean (standard deviation)

TABLE 6. Mean anterior shear exerted by longus capitis and colli as an expression of specific tension (K)

Cervical level C0/1 C1/2 C2/3 C3/4 C4/5 C5/6 C6/7 C7/T1 T1/2

Longus capitis Males C3 -0.06K (0.04) -0.07K (0.02) 0.03K (0.03) C4 -0.05K (0.04) -0.06K (0.02) 0.03K (0.02) 0.03K (0.02) C5 -0.12K (0.08) -0.13K (0.04) 0.04K (0.03) 0.04K (0.03) 0.06K (0.05) C6 -0.15K (0.11) -0.16K (0.06) 0.03K (0.02) 0.03K (0.03) 0.06K (0.03) 0.10K (0.07) Subtotal -0.39K (0.08) -0.41K (0.06) 0.13K (0.02) 0.10K (0.02) 0.12K (0.04) 0.10K (0.07) Females C3 -0.06K (0.04) -0.06K (0.02) 0.03K (0.03) C4 -0.03K (0.03) -0.03K (0.01) 0.02K (0.01) 0.02K (0.01) C5 -0.08K (0.06) -0.09K (0.03) 0.03K (0.02) 0.03K (0.02) 0.04K (0.03) C6 -0.10K (0.07) -0.11K (0.04) 0.02K (0.02) 0.02K (0.02) 0.04K (0.02) 0.06K (0.04) Subtotal -0.27K (0.05) -0.29K (0.04) 0.09K (0.02) 0.06K (0.02) 0.08K (0.03) 0.06K (0.04)

Longus colli Males SO -0.17K (0.01) -0.05K (0.01) -0.06K (0.01) -0.02K (0.01) 0.00K (0.01) Vertical -0.05K (0.01) -0.07K (0.02) -0.05K (0.01) -0.01K (0.01) 0.03K (0.01) 0.06K (0.01) 0.02K (0.00) IO 0.00K (0.00) 0.01K (0.00) 0.00K (0.00) Subtotal -0.17K (0.02) -0.10K (0.01) -0.13K (0.02) -0.06K (0.01) -0.01K (0.01) 0.02K (0.01) 0.07K (0.01) 0.02K (0.01) Females SO -0.17K (0.01) -0.06K (0.01) -0.06K (0.01) -0.02K (0.01) 0.00K (0.01) Vertical -0.04K (0.01) -0.06K (0.01) -0.04K (0.01) -0.01K (0.01) 0.02K (0.00) 0.04K (0.01) 0.02K (0.00) IO 0.00K (0.01) 0.01K (0.00) 0.00K (0.00) Subtotal -0.17K (0.03) -0.09K (0.01) -0.12K (0.02) -0.06K (0.01) -0.01K (0.01) 0.02K (0.01) 0.05K (0.01) 0.02K (0.01)

Abbreviations: SO, Superior oblique; IO, Inferior oblique Values presented are mean (standard deviation) Negative values (-) represent posterior shear

Longus capitis Longus colli 0.30 0.25 0.20 0.15 0.10 0.05

0.00

Males Males Males Males Males

Females Females Females Females Females C2/3 C3/4 C4/5 C5/6 C6/7

FIGURE 4. Peak flexion torque estimates (Nm) based on a specific tension of 15 Nm2 (a mid- range value for data derived from MRI volumes (Fukunaga et al., 1996)). Note values are for a single muscle, and can be doubled to represent bilateral action.

Longus capitis Longus colli 45.0 40.0 35.0 30.0 25.0 20.0 15.0 10.0 5.0

0.0

Males Males Males Males Males Males Males Males Males

Females Females Females Females Females Females Females Females Females C0/1 C1/2 C2/3 C3/4 C4/5 C5/6 C6/7 C7/T1 T1/2

FIGURE 5. Peak compression estimates (N) based on a specific tension of 15 Nm2 (a mid- range value for data derived from MRI volumes (Fukunaga et al., 1996)). Note values are for a single muscle, and can be doubled to represent bilateral action.

Longus capitis Longus colli 10.0 8.0 6.0 4.0 2.0 0.0 -2.0 -4.0 -6.0 -8.0

-10.0

Males Males Males Males Males Males Males Males Males

Females Females Females Females Females Females Females Females Females C0/1 C1/2 C2/3 C3/4 C4/5 C5/6 C6/7 C7/T1 T1/2

FIGURE 6. Peak shear estimates (N) based on a specific tension of 15 Nm2 (a mid-range value for data derived from MRI volumes (Fukunaga et al., 1996)). Positive values represent anterior, and negative values posterior shear. Note values are for a single muscle, and can be doubled to represent bilateral action.

DISCUSSION

This study describes the fascicular morphology and peak force capabilities of longus capitis and colli, highlighting a complex arrangement of small fascicles with correspondingly small force capacity. The fascicular anatomy of the longus muscles highlights that these muscles span multiple motion segments, with greater muscle bulk at higher cervical levels. To our knowledge this is the first time the fascicular anatomy of longus colli has been described, showing a variable fascicular arrangement and very small individual fascicles (Table 2). The majority of longus colli by volume was found in the superior oblique portion. In terms of volume and PCSA the relative size of each portion roughly followed a ratio of 3:2:1 (superior oblique: vertical: inferior oblique). The muscle volumes shown on MRI were substantially larger than those found during dissection, highlighting the value of obtaining in vivo muscle volumes. This reflects changes due to age (Narici et al., 2003) and embalming (Stickland,

1975), which are important to address when utilising the data for force calculations

(Fukunaga et al., 2001, Gadeberg et al., 1999).

To assist in interpreting these force values, a human head (approx. 5kg) would produce axial compression of ~50N, and with a one-centimetre moment arm would exert a moment of

~0.5 Nm. Peak torque capacity for both muscles was calculated to be greatest at C2/3 (0.5

Nm acting bilaterally), and negligible below the level of C5 (<0.2 Nm acting bilaterally). This is generally comparable with previous work (Vasavada et al., 1998), which can be calculated as 0.68 Nm (without reference to a specific level). That the peak torque capacity for longus colli was also at C2/3 is perhaps more surprising, and reflects greater muscle volume in the superior oblique portion. This is an advance on previous work, which modelled the peak force capacity of each portion equally – attributing 10 N to each of the superior oblique, vertical and inferior oblique portions (Vasavada et al., 1998). Combined peak shear 22 estimates are negligible (<20 N acting bilaterally). Peak compression estimates were low

(<80 N).

As the effect of compression is relevant to models of stability, the low peak force estimates are particularly interesting. Simulated neck muscle activity has been shown to stabilise the upper cervical spine (occiput-C2) in a mechanical model including longus capitis (Kettler et al., 2002). This model used an axial force of 15 N for each longus capitis, acknowledging that this was an estimate - as physiological force data were not available. This study provides such data, estimating the peak compressive force capacity of longus capitis as 1.38K

(occiput-C2, males). Using a specific tension of 15 Nm2, this equates to a physiological peak of 20.7N. Thus, to provide 15 N of axial compression longus capitis would have to act at 72% of maximal capacity. While within physiological limits, this is in stark contrast to modelling indicating deep muscles in the lumbar spine can generate stability with just 1-3% of the maximum voluntary contraction (Cholewicki and McGill, 1996). In this way, the ability of longus capitis (and by association, longus colli) to stabilise the cervical spine may have been overestimated. Or at least, if the longus muscles contribute to stability, perhaps they are more likely to do so with higher levels of phasic activity, in contrast to more traditional views of ‘postural’ low level tonic activity. This would be consistent with their histological composition and force capabilities.

It is an apparent contradiction that the longus muscles are capable of only small peak forces, yet are considered important during voluntary movement in biomechanical (Winters and

Peles, 1990), EMG (Conley et al., 1995, Falla et al., 2003, Fountain et al., 1966, Vitti et al.,

1973), and histological study (Boyd-Clark et al., 2001, Cornwall and Kennedy, 2015, Miller et al., 2016). This may be explained by the mechanics of the upright position: the head-neck

23 complex behaves like a well-balanced inverted pendulum, with the centre of mass of the head lying anterior to the neck (Winters and Peles, 1990). In this context, the longus muscles may not need to produce large forces to usefully participate in voluntary motion of the cervical spine, particularly at higher vertebral levels. It is more difficult to imagine them contributing to motion in non-upright positions (e.g. supine). Another point to consider is that the infra and suprahyoid muscles may contribute to cervical flexion. While small in size, these muscles have large moment arms (Falla et al., 2006, Vasavada et al., 1998). Their contribution could be significant at higher cervical levels where the sternocleidomastoid no longer exerts a flexion moment, and the longus muscles are only capable of generating small forces.

It is worth considering the implications for clinical assessment and therapy reported to target the longus muscles, in particular the CCFT described by Jull et al (2008b). The CCFT is described as a small controlled nodding action performed in supine with the head supported (Jull et al., 2008b), to test the action of longus capitis and colli in stabilising the cervical spine (Falla et al., 2004, Jull et al., 2008b). The test motion appears within the small flexion torque capacity of the longus muscles, but it is less clear if longus muscle activity is an effective source of stability. As discussed, longus capitis and colli appear mechanically weak and histologically unsuited to producing stability through low-load endurance tasks.

More attention to how they contribute to voluntary movements in the upright position may be valuable. It also seems possible that the clinical benefits derived from cranio-cervical flexion testing and exercise are not tied to the concept of stability, and other mechanisms may play a greater role. Consistent with this view, clinical improvements in the CCFT have been achieved with interventions such as passive movement (Lluch et al., 2014) and proprioception training (Gallego Izquierdo et al., 2016) that do not specifically address 24 activity of the longus muscles. Overall, a great deal of evidence indicates that cranio-cervical flexion is a useful tool for a range of neck-related disorders. However, this work highlights that there is more to learn about the mechanisms by which these clinical benefits are achieved.

This research has several limitations to consider. A more complete discussion of the methods, their advantages and limitations has been previously published (XX). The findings are limited to estimating the peak force generating capabilities of the longus muscles in the neutral position, and the sagittal plane. How these forces change with head and neck position has been examined elsewhere (Vasavada et al., 1998). The biomechanical model presented focuses on a relatively simple calculation of peak force capability, and does not represent forces produced during normal motion. Perhaps most importantly – however carefully considered – our results remain an estimate of peak force capabilities. Many other factors such the elastic properties of muscle tissue (Ettema and Huijing, 1990, Winters,

1990) affect peak force production, but are not considered in this study. Rather, this study focuses on the factors we consider most important in estimating peak force capacity, namely accurate modelling of the fascicular muscle attachments and in vivo muscle volumes from young healthy volunteers.

CONCLUSIONS

This research reveals the fascicular anatomy and peak force capacity of longus capitis and colli with relation to the individual motion segments of the cervical spine. These data inform our understanding of what forces these muscles are, and are not, capable of generating – knowledge relevant to academics and clinicians alike. Overall, these muscles are small, with a complex fascicular arrangement, and capable of only small peak flexion torque or compression forces. This suggests that longus capitis and colli have a limited capacity to contribute to cervical stability via traditional (compressive) mechanisms, and implies that a closer look at how cranio-cervical flexion exercises produce clinical benefits could be valuable.

Acknowledgements

We are grateful for the generosity of the body donors and their families without whom cadaveric research would not be possible, and the volunteers who contributed to the MRI study. We also acknowledge the strong contribution of Dr Susan Mercer in the early stages of this work.

REFERENCES

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LIST OF TABLES

TABLE 1. Fascicular anatomy and morphology of longus capitis TABLE 2. Fascicular anatomy and morphology of longus colli TABLE 3. Comparison of dissection and MRI muscle volumes TABLE 4. Mean peak flexion torque exerted by longus capitis and colli as an expression of specific tension (K) TABLE 5. Mean peak compression exerted by longus capitis and colli as an expression of specific tension (K) TABLE 6. Mean anterior shear exerted by longus capitis and colli as an expression of specific tension (K)

LIST OF FIGURES

FIGURE 1. Anterior view of longus capitis and colli. Note the superficial aponeurosis in the mid-section of longus capitis, and the superior muscle belly (*). FIGURE 2. Lateral view of longus capitis showing the fascicles attaching to the anterior tubercles of C3, C4, C5 and C6 respectively. Note how the fascicles to C5 and C6 fuse at the aponeurosis (*). FIGURE 3. Anterolateral view of longus colli illustrating fascicles of the superior oblique superiorly detached from the anterior tubercle of C1. Note their small size and mix of muscle and tendinous tissue. FIGURE 4. Peak flexion torque estimates (Nm) based on a specific tension of 15 Nm2 (a mid- range value for data derived from MRI volumes (Fukunaga et al., 1996)). Note values are for a single muscle, and can be doubled to represent bilateral action. FIGURE 5. Peak compression estimates (N) based on a specific tension of 15 Nm2 (a mid- range value for data derived from MRI volumes (Fukunaga et al., 1996)). Note values are for a single muscle, and can be doubled to represent bilateral action. FIGURE 6. Peak shear estimates (N) based on a specific tension of 15 Nm2 (a mid-range value for data derived from MRI volumes (Fukunaga et al., 1996)). Positive values represent anterior, and negative values posterior shear. Note values are for a single muscle, and can be doubled to represent bilateral action.