SPINE Volume 29, Number 7, pp E139E144

2004, Lippincott Williams & Wilkins, Inc.

Kinematics of the Upper Cervical Spine in Rotation

In Vivo Three-Dimensional Analysis
Takahiro Ishii, MD,* Yoshihiro Mukai, MD,* Noboru Hosono, MD, PhD,*
Hironobu Sakaura, MD,* Yoshikazu Nakajima, PhD, Yoshinobu Sato, PhD,
Kazuomi Sugamoto, MD, PhD,* and Hideki Yoshikawa, MD, PhD*

Study Design. Kinematics of the upper cervical spine

during head rotation were investigated using three-dimensional magnetic resonance imaging (MRI) in healthy
volunteers.
Objectives. To demonstrate in vivo intervertebral coupled motions of the upper cervical spine.
Summary of Background Data. Although various in
vivo and in vitro studies have identified the normal movement patterns of the upper cervical spine, no previous
studies have accurately analyzed in vivo three-dimensional intervertebral motions of the upper cervical spine
during head rotation.
Methods. Fifteen healthy volunteers underwent threedimensional MRI of the upper cervical spine using a 1.0-T
imager in progressive 15 steps during head rotation.
Segmented three-dimensional MRIs of each vertebra in
the neutral position were superimposed over images
taken at other positions, using voxel-based registration.
Relative motions between occiput (Oc) and atlas (C1) and
between C1 and axis (C2) were measured and described
with 6 degrees of freedom by rigid body Euler angles and
translations.
Results. Mean (! SD) maximum angles of axial rotation in OcC1 and C1C2 were 1.7 ! 1.5 and 36.2 ! 4.5
to each side, respectively. Increases in angle of axial rotation in C1C2 became smaller with increased head rotation, indicating axial rotation in C1C2 displayed nonlinear motion. Coupled lateral bending with axial rotation
was observed in the direction opposition to that of axial
rotation in OcC1 (mean, 4.1 ! 1.4) and C1C2 (mean, 3.8
! 3.0). Coupled extension with axial rotation occurred at
both C0 C1 (mean, 13.3 ! 4.9) and C1C2 (mean, 6.9 !
3.0).
Conclusions. We developed an innovative in vivo
three-dimensional motion analysis system using threedimensional MRI. In vivo coupled motions of the upper
cervical spine investigated using this system supported
the results of the previous in vitro study. [Key words:
kinematics, coupling motion, atlantoaxial joint, volume
registration] Spine 2004;29:E139 E144

The upper cervical spine represents quite a unique anatomy compared with other regions of the spine and displays a complicated combination of motions, including
flexion extension, lateral bending, and axial rotation. In
head rotation, the upper cervical spine offers a large
amount of axial rotation combined with lateral bending
and flexion extension, best known as coupled motions.
In vitro studies have previously been the only method for
obtaining quantitative data on three-dimensional (3D)
intervertebral motions.1 However, the lack of physiologic tonus of musculature makes the results of in vitro
study impractical.
In vivo 3D motions of the upper cervical spine have
remained largely unexplored. We have developed a
unique system for motion analysis and succeeded in determining in vivo coupled motions of the upper cervical
spine during head rotation. The purpose of this study
was to accurately demonstrate for the first time the in
vivo 3D intervertebral motions of the upper cervical
spine during rotation.
Materials and Methods
Study participants comprised 15 healthy volunteers (8 men, 7
women) with a mean age of 24.3 years (range, 2231 years).
None of these volunteers had neck pain or a medical history of
cervical disorders. The system of 3D motion analysis developed
in our laboratory (Virtual Place M series, Medical Imaging
Laboratory, Tokyo, Japan and Poly-editor, Division of Functional Diagnostic Imaging, Biomedical Research Center, Osaka
University Medical School) consists of the following steps: acquisition of 3D-magnetic resonance imaging (MRI), segmentation, voxel-based registration, and motion analysis, in which a
mathematical description of the motions and relative motions
of individual upper cervical spines was derived by computing
the rigid transformation required to superimpose the 3D MRI.

Acquisition of 3D MRI. Magnetic resonance images were

From the *Department of Orthopaedic Surgery, Osaka University

Graduate School of Medicine; and Interdisciplinary Image Analysis,
Osaka University Graduate School of Medicine, Osaka, Japan.
Acknowledgment date: May 30, 2003. First revision date: August 7,
2003. Acceptance date: October 27, 2003.
The manuscript submitted does not contain information about medical
device(s)/drug(s).
No funds were received in support of this work. No benefits in any
form have been or will be received from a commercial party related
directly or indirectly to the subject of this manuscript.
Address correspondence to Takahiro Ishii, MD, Department of Orthopaedic Surgery, Osaka University Graduate School of Medicine, 2-2
Yamada-Oka, Suita, Osaka 565-0871, Japan; E-mail:
ishii-takahiro88@umin.ac.jp

taken using a 1.0-T imager (Signa LX, General Electric, Milwaukee, WI). A torso phased array coil was settled in front and
behind the neck in order to receive more signals. The 3D images
were obtained using 3D-fast GRASS (gradient recalled acquisition in the steady state) pulse sequence (repetition time/echo
time, 8.0/3.3), 1.5 mm slice thickness, and no interslice gap.
The flip angle was 10, and a 24-cm field-of-view was used
(imaging matrix, 256 " 224). Imaging time was approximately
5 minutes for one position.
Subjects were placed supine on the MRI table and asked to
rotate their heads from neutral to maximum rotation in 15
steps (0, 15, 30, 45, 60, and maximum) while 3D images
were obtained for 11 positions. Subjects always rotated their
head on a plane perpendicular to the MRI table by keeping
E139

E140 Spine Volume 29 Number 7 2004

Figure 1. Process of voxel-based registration.

both of their eyes on the positioning beam of the MRI machine
throughout head rotation, and their shoulders were fixed to the
table with the band. Degree of head rotation was measured on
axial scout-view images as the angle between a line perpendicular to the MRI table and a line through the nasal septum and
occipital protuberance.

Segmentation. Segmentation is defined as extracting a range

of images required for processing. Contours of the upper cervical spine in the neutral position were semiautomatically extracted from 3D MRIs by intensity thresholding techniques.

Voxel-Based Registration. Voxel-based registration represents a method for determining relative positions between volume images represented at different coordinates, using a corresponding method based on correlation between voxel values.
The correlation coefficient was used as a measure of similarity.
Using this method, a segmented 3D MRI of the vertebra in the
neutral position was superimposed over images for each position. Relative motion of the spine was then calculated by starting from initial transformation parameters and finally finding
the parameters allowing maximal correlation of the two images
(Figure 1).
Validation of Voxel-Based Registration Accuracy. The
accuracy of voxel-based registration for the cervical spine on
3D MRI underwent preliminary validation in in vivo experiments using phantom MRI. A phantom with markers, comprising four high precision ceramic balls, was attached to the head
through a diving mask and was used to determine gold standard positions. The phantom was scanned at various orientations, and all scans were registered to the reference scan. Translational and rotational errors were calculated for voxel-based
registration of the occiput, and the accuracy was validated with
reference to the root mean square distance calculated by corresponding marker sets. Mean absolute rotational error was
0.24 for flexion extension, 0.31 for lateral bending, and
0.43 for axial rotation. Mean absolute translational error was
0.52 mm for superoinferior translation, 0.51 mm for anteroposterior translation, and 0.41 mm for lateral translation.
Coordinate System. The absolute spatial coordinate system
in MRI space was defined as shown in Figure 2a. Motions of C1

Figure 2. A: Absolute spatial coordinate system. The positive xaxis is directed to the left, perpendicular to the sagittal plane. The
positive y-axis is directed superiorly, and the positive z-axis is
oriented anteriorly. B: Anatomic orthogonal coordinate system for
Oc and C1. The z-axis of Oc was parallel to the line connecting
anterior and posterior borders of the foramen magnum, with anterior considered positive. The y-axis was defined as perpendicular to the z-axis, with superior being positive. The x-axis was
positive to the left. Similar to Oc, the anatomic orthogonal coordinate system of C1 was defined using two points: the posteroinferior border of the anterior arch and the anteroinferior border of
the posterior arch. Origins were located at the anterior border of
the foramen magnum on Oc, and the posteroinferior border of the
anterior arch on C1.
and C2 in MRI space were measured using the absolute spatial
coordinate system.
The anatomic orthogonal coordinate systems of Oc and C1
were defined as described by Panjabi et al (Figure 2b).2 Relative
motions between Oc and C1 and between C1 and C2 were
measured on the anatomic orthogonal coordinate system and
described with 6 degrees of freedom by rigid body Euler angles
and translations.3

Visualization. Surface models of the upper cervical spine for

each participant were reconstructed from 3D MRI data using
the marching cubes algorithm in the Visualization Toolkit.4,5
Upper cervical motions were visualized in animations using
surface bone models and the resulting calculated motions were
validated.

Results
Movement of C1 and C2 on the Absolute Spatial
Coordinate System
Movements of C1 and C2 on the absolute spatial coordinate system are given in Figure 3. The mean (! SD)
angle of axial rotation of the head from neutral to maximum was 72.1 ! 5.7 on the MRI coordinate system. At
maximum head rotation, mean axial rotations of C1 and

Kinematics of Upper Cervical Spine Ishii et al E141

with axial rotation was observed at OcC1 (mean, 4.1 !

1.4) in the direction opposing axial rotation. Coupled
extension with axial rotation occurred at OcC1 (mean,
13.3 ! 4.9), irrespective of the direction of head rotation. Mean maximum axial rotation between C1 and C2
was 36.2 ! 4.5 to each side. Axial rotation of C1 with
respect to C2 was found to be nonlinear, with increases
in angle of axial rotation for C1C2 becoming smaller
with increased head rotation. Similarly to OcC1, lateral
bending in the opposite direction to axial rotation was
coupled with axial rotation at C1C2 (mean, 3.8 !
3.0). Extension was also coupled with axial rotation at
C1C2 (mean, 6.9 ! 3.0; Figure 5).
Coupled lateral translation at the origin of the anatomic orthogonal coordinate system with axial rotation
was observed in the same direction as axial rotation for
OcC1 (mean, 2.1 ! 0.6 mm) and C1C2 (mean 3.4 !
1.0 mm). Coupled anteroposterior and superoinferior
translation of Oc relative to C1 with axial rotation was
observed in anterior (mean, 0.7 ! 0.5 mm) and superior
(mean, 1.5 ! 0.6 mm) directions. Coupled anteroposterior and superoinferior translation of C1 relative to C2
with axial rotation occurred in posterior (mean, 0.3 !
0.5 mm) and inferior (mean, 0.9 ! 0.6 mm) directions.
Discussion

Figure 3. Movement of C1 (A) and C2 (B) on the absolute spatial

coordinate system. Degree of head axial rotation was plotted on
the x-axis, whereas degree of rotational movement of C1 and C2
along each axis on the MRI coordinate system was plotted on the
y-axis. Approximate curves for movements were drawn.

C2 to one side were 70.8 ! 5.6 and 34.2 ! 6.6, respectively. Coupled lateral bending of C1 (mean, 6.8 ! 4.1)
and C2 (mean, 11.3 ! 3.4) with axial rotation was
observed in the same direction as the axial rotation. Coupled flexion with axial rotation occurred at both C1
(mean, 6.0 ! 5.1) and C2 (mean, 5.7 ! 4.4), irrespective of direction of head rotation.
OcC1 and C1C2 Intervertebral Movement
Intervertebral movements at OcC1 and C1C2 are
shown in Figure 4. Mean axial rotation between Oc and
C1 was 1.7 ! 1.5 to each side. Coupled lateral bending

The in vivo kinematics of the cervical spine have predominantly been investigated using two-dimensional images
under conventional computed tomography (CT) and
MRI.6 8 These studies have only shown the magnitudes
of axial rotation, with no detailed descriptions of complex coupled motions. Biplanar radiography was the first
tool to indicate in vivo coupled motions.9,10 However,
the method was unreliable because of the large potential
for intraobserver and interobserver variability in tracking bony landmarks on plain radiographs.11 Furthermore, high doses of radiation make the analysis of continuous movements unfeasible using that method. Some
authors have used opto-electronic scanners tracking skin
markers with small infrared-emitting diodes.12 However, these methods failed to yield quantitative data because of discrepancies in the motions of skin markers and
the cervical spine.
Recently, some studies of in vivo 3D kinematics using
3D CT or 3D MRI have undertaken motion analyses of
foot and hand joints.1315 No previous studies of spine
kinematics have used such methods. Although 3D MRI
is inferior to 3D CT in accurate imaging of bone, we used
3D MRI in the present in vivo studies to avoid subject
exposure to radiation. Surface-based registration,16
which is a technique to register two rigid 3D surface bone
models, has previously been used for in vivo studies of
3D kinematics.1315 However, surface-based techniques
are not appropriate for 3D MRI, as the low resolution of
3D MRI complicates the extraction of exact bone contours. Conversely, voxel-based techniques allow registration by making use of relationships between voxel
intensities within images,17 and accuracy does not de-

E142 Spine Volume 29 Number 7 2004

Figure 4. Intervertebral movements at OcC1 (A and C) and C1C2 (B and D). Degree of head axial rotation was plotted on the x-axis,
whereas degree of rotational movement along each axis on anatomic orthogonal coordinate system and length of translational movement
at OcC1 or C1C2 was plotted on the y-axis. Approximate curves for movements were drawn.

pend on the precision of extracted bony contours. We

therefore used voxel-based registration for kinematics
and developed a new noninvasive system of 3D motion
analysis. The present study succeeded in achieving reliable measurement of in vivo coupled motions of the upper cervical spine during head rotation.
Previous representative data for axial rotation of the
upper cervical spine are shown in Table 1. The complete
absence of axial rotation between Oc and C1 has been
mentioned in classic cadaveric studies.18 20 However,
recent investigations have observed unilateral axial rotation in the range of #4.0 to 7.3.6,7,10,21 The present
results confirm in vivo results from two-dimensional
CT.6,7 One previous in vivo study using biplanar radiography identified axial rotation between Oc and C1 in the
opposite direction to head rotation,10 which is difficult to
interpret anatomically. In our study, axial rotation between Oc and C1 was in the same direction as head

rotation, which is consistent with most previous reports.

The results obtained from biplanar radiography might
therefore have arisen because of methodologic
inaccuracies.
Axial rotation at C1C2 has been described as comprising approximately 60% of the entire cervical spine,
with a unilateral range of 32.2 to 60.6,7,10,18 21 Our
results for axial rotation at C1C2 (36.3) resemble
those of previous in vitro studies by Panjabi et al21 and in
vivo studies.6,7,10 The approximated curve for axial rotation of C1 relative to C2 was found to be nonlinear
(Figure 4). This means that the C1C2 joint plays a major role in the initial phase of head rotation, followed by
subaxial rotation. This nonlinear pattern of rotation can
be explained by differing compliance to rotational stress
between the atlantoaxial and subaxial joints.
Table 1. Comparison of the Mean Range of Axial
Rotation on One Side ()
C0C1

Figure 5. Intervertebral movements at C1C2 viewed from posterior. In left rotation, right lateral bending and extension were
coupled. In right rotation, left lateral bending and extension were
coupled.

In vitro
Fick (1904)
Werne (1959)
W&P (1978)
Panjabi (1988)
In vivo
Dvorak (1987)
Penning (1987)
Iai (1989)
present study

Cadaver
Cadaver
Cadaver
Cadaver
CT
CT
Bi-plane x-ray
3 D MRI

C1C2

0
0
0
7.3

60
47
47
38.9

4
1
#4
1.7

41.5
40.5
38
36.3

Kinematics of Upper Cervical Spine Ishii et al E143

Table 2. Comparison of Mean Ranges of Coupled Rotational Motion (Axial Rotation [AR], Lateral Bending [LB], and
FlexionExtension [FE]) on One Side ()
C0C1
Main AR
In vitro study
Panjabi et al (2001)
In vivo studies
Iai et al (1989)
Present study

Coupled LB

Coupled FE

Main AR

Coupled LB

Coupled FE

4.9

1.8

#11.7

28.4

3.1

#3.5

#4
1.7

4.1

#10
#13.4

38
36.3

11
3.8

#6.8

Cadaver
Bi-plane x-ray
3D MRI

C1C2

Coupled lateral bending ($) represents the opposite direction of axial rotation. Coupled flexion extension (#) represents extension.

Previous representative data of intervertebral coupled

motions with axial rotation in the upper cervical spine
are shown in Tables 2 and 3. Few studies have provided
quantitative information for intervertebral coupled motions in the upper cervical spine.1,2,10,22 In our study,
coupled lateral bending in the opposite direction to axial
rotation and coupled extension were demonstrated at
both OcC1 and C1C2. These results confirm those of
previous in vitro study by Panjabi et al,1 but not the
biplanar examination, except for coupled extension at
OcC1 and coupled lateral bending at C1C2.10 In the
subaxial cervical spine, lateral bending is combined with
rotation in the same direction.23 We speculate that, to
maintain horizontal positioning of the head, the upper
cervical spine compensates for subaxial ipsilateral bending during head rotation by contralateral bending. Regarding coupled translation at C0 C1, lateral translation of Oc with respect to C1 takes place in the same
direction as rotation.2,7 We also found lateral translation
of Oc (2.1 mm) identical to that reported in an in vitro
study by Oda et al.2 Coupled inferior translation of C1 in
relation to C2 was seen to take place during rotation in
our study. Henke described this as a double-threaded
screw mechanism. 24 The traditional phenomenon
known as screw movement was first indicated quantitatively using sophisticated methods, but it remains unclear whether this can be attributed to biconvexity of the
articulations.
Our innovative system facilitates noninvasive, quantitative, and accurate in vivo 3D motion analyses. Moreover, motion 1of the cervical spine can be visualized in
animations by reconstructing surface bone models. This

method does, however, contain three weaknesses: 1)

MRI did not follow real continuous motion, but rather
progressive steps of 15 rotation; 2) the loads exerted by
subjects to produce rotations in vivo could not be quantified as in vitro studies1,2,10,22,25,26; and 3) subjects were
supine, not in the upright position. The differences of
postures may have an effect on spinal motions. Further
investigations using open MRI, which allows the cervical
spine to be scanned with the patient in the upright position, would resolve one of these drawbacks.
Key Points
In vivo three-dimensional intervertebral motion
of the upper cervical spine in rotation was investigated using a newly developed system of threedimensional motion analysis.
Coupled lateral bending with axial rotation was
observed in the opposite direction to that of axial
rotation at OcC1 (mean, 4.1 ! 1.4) and C1C2
(mean, 3.8 ! 3.0).
Coupled extension with axial rotation occurred
at C0 C1 (mean, 13.3 ! 4.9) and C1C2 (mean,
6.9 ! 3.0), irrespective of the direction of head
rotation.

Acknowledgment
The authors thank Ryoji Nakao for assistance in programming computer software, Mitsuhiro Shiotani for assistance in producing MRIs, and Sadayuki Miyatani for
assistance in producing the device for motion analysis.

Table 3. Comparison of Mean Ranges of Coupled Translational Motion (SuperoInferior [SI], Lateral [L], and
Anteroposterior [AP] Translation) on One Side (mm)
C0C1

In vitro study
Oda et al (1991)
In vivo study
Present study

C1C2

Modality

Coupled SI

Coupled L

Coupled AP

Cadaver

1.6

2.1

#0.3

3D MRI

1.5

2.1

0.7

Coupled SI

Coupled L

Coupled AP

0.7

4.9

#0.9

3.4

#0.3

Translation ($) represent superior for superoinferior, the same direction in the axial rotation for lateral, and anterior for anteroposterior.

E144 Spine Volume 29 Number 7 2004

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