2016 Anatomy and Cervical Dystonia

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J Neural Transm

DOI 10.1007/s00702-016-1621-7

HIGH IMPACT REVIEW IN NEUROSCIENCE, NEUROLOGY OR PSYCHIATRY - REVIEW ARTICLE

Anatomy and cervical dystonia


‘‘Dysfunction follows form’’

L. Tatu1,2 • W. H. Jost3

Received: 6 June 2016 / Accepted: 6 September 2016


Ó Springer-Verlag Wien 2016

Abstract At first glance, cervical dystonia might be an Introduction


illustration of the well-known proposition ‘‘function fol-
lows form’’. Nevertheless, cervical dystonia is a highly There is an age-old question concerning form and function,
non-physiological condition, which cannot be reproduced anatomy and physiology. The relationships between these
by healthy subjects and does not respond to the usual two major branches of medicine are still a matter of debate.
physiological rules. ‘‘Dysfunction follows form’’ might be The aphorism ‘‘form follows function’’, a principle asso-
the most accurate aphorism to define cervical dystonia. ciated with architecture, is frequently applied to anatomy
Taking into account this situation and recent insights, the (Tubbs 2015). The reverse alliteration ‘‘function follows
anatomic approach needs to be adapted to allow a better form’’ is more accurately used nowadays (Bergman 2015).
understanding of semiology and to improve botulinum Cervical dystonia can be regarded as an example of this
toxin therapy. In this review dealing with a new approach old debate. In the last decade, anatomy has reappeared as a
to cervical dystonia, we develop some practical anatomical major point in the management of cervical dystonia,
concepts concerning the head and neck complex. Knowl- thereby reopening the discussion between form and func-
edge of cervical spine and muscular dysfunctions in cer- tion. The ‘‘collis caput concept’’, a practical semiologic
vical dystonia is an essential stage in treating cervical analysis procedure for cervical dystonia, is, for example,
dystonia patients with botulinum toxin. mainly built on anatomic data and muscle functions (Re-
ichel 2011).
Keywords Cervical dystonia  Botulinum toxin  Based on well-known anatomic and biomechanic data,
Anatomy  Cervical muscles  Muscular function movements of the head and neck are an interesting example
of the alliteration ‘‘function follows form’’. At first glance,
cervical dystonia might be another illustration of this
condition as well. Nevertheless, cervical dystonia is a
highly non-physiological condition. Numerous postures
and abnormal movements observed in cervical dystonia
cannot be reproduced by healthy subjects and do not
respond to usual physiological rules. Then, ‘‘dysfunction
follows form’’ might be the most accurate aphorism to
& L. Tatu define cervical dystonia. Taking into account this situation,
laurent.tatu@univ-fcomte.fr
the anatomic approach needs to be adapted to allow a better
1
Department of Anatomy, University of Franche-Comté, understanding of cervical dystonia semiology.
Besançon, France For a long time, botulinum toxin has been the preferred
2
Department of Neuromuscular Diseases, CHRU Besançon, method in treating cervical dystonia (Wissel et al. 2001).
Besançon, France Nevertheless, failures in botulinum toxin exist and some of
3
Department of Neurology, University of Freiburg, Freiburg, the reasons for these unsatisfactory responses need to be
Germany elucidated (Jinnah et al. 2016). Misunderstanding of

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L. Tatu, W. H. Jost

functional anatomy is undoubtedly one of these factors. To


improve botulinum toxin therapy, in this review, we pro-
pose some practical anatomic data applied to cervical
dystonia.

Functional anatomy of cervical spine applied Head and C1


to cervical dystonia
C2

Because postures and abnormal movements observed in C3-C7


cervical dystonia are highly non-physiological conditions,
the question is: do the standard physiological biomechan-
ical data concerning the head and neck movements help us
in cervical dystonia?
Some authors have been working on cervical spine
biomechanics and elaborating theories on head and neck
movements (Kapandji 2008). We can argue that these Fig. 1 Anatomic organization of ‘‘Head and neck complex’’ applied
biomechanic models are not really helpful in cervical to cervical dystonia
dystonia. They concern only normal situations and healthy
subjects. Moreover, they are so sophisticated that it is With regard to the semiology, anatomical landmarks of
difficult to use them in clinical practice. the ventral part of the neck are of major interest. Jugular
In cervical dystonia patients, we need information to notch (Incisura jugularis sternalis), and laryngeal promi-
help us analyze the semiologic patterns of abnormal nence (Adam’s apple) should be considered to define which
movement and to select the involved muscles. The most part of the ‘‘head and neck complex’’ is involved in the
practical vision of abnormal movements of the ‘‘head and abnormal movement and posture. In cases of head rotation
neck complex’’ is to consider two different parts in this or head lateroflexion, these two structures remain aligned.
complex: the upper level ‘‘head and C1’’ and the lower This condition corresponds to the ‘‘caput’’ status of the
‘‘C3–C7’’. The two levels are able to move independently, ‘‘collis caput complex’’. If these structures are no longer
the upper one in relation to the lower one and the lower aligned, the neck is involved in the abnormal movement as
one in relation to the thoracic spine. In this situation, C2 well, corresponding to the ‘‘collis’’ condition of the ‘‘collis
acts as a kind of ‘‘fixed point’’ due to the numerous caput complex’’. In this condition, we can claim that the
muscles inserted on its spinous process (i.e., obliquus main muscles involved act on the ‘‘C3–C7 level’’ (Fig. 2a).
capitis inferior, rectus capitis major, semispinalis cervicis, In the sagittal plane, the meatus acusticus externus and
multifidus). This functional division of the ‘‘head and the clavicula are useful anatomical landmarks as well. In
neck complex’’ is one of the anatomic basics of the case of ante- or retroflexion, if only the ‘‘head and C1
‘‘collis caput complex’’ (Reichel 2011; Jost and Tatu complex’’ is concerned, then meatus acusticus externus
2015) (Fig. 1). stays in projection of the clavicula. If the ‘‘C3–C7 level’’ is
From a semiologic point of view, the question is to involved in cervical dystonia, then meatus acusticus
define in cervical dystonia which level is mainly involved externus’ projection is in front of or behind the clavicular
in the abnormal movement. It may concern only ‘‘the head (Fig. 2b).
and C1’’ level without movements of ‘‘C3–C7’’. On the Whatever the guidance (electromyography or/and
other hand, the abnormal movement may concern mainly ultrasonography) of botulinum toxin injections, knowledge
‘‘C3–C7’’. In this lower part, some segments (e.g., C3–C4) of topographic landmarks of the dorsal and lateral aspects
can be more involved than the others, depending on the of the neck is essential. The posterior triangle of the neck is
cervical dystonia type. the key of lateral region of the neck. The triangle is
delimited by the posterior edge of the sternocleidomas-
toideus muscle and the anterior edge of the trapezius
Knowledge of topographic anatomy is muscle. The base of the triangle is the middle third of the
fundamental clavicula, and the apex of the triangle, behind the mastoid
process, is a narrow area where sternocleidomastoideus and
In cervical dystonia, topographic anatomy is relevant to trapezius muscles meet. In this triangle, splenius capitis,
two main topics: semiologic analysis and guidance of levator scapulae and scalenus medius muscles can be
botulinum toxin injections. injected. Nevertheless, the morphology of the posterior

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Anatomy and cervical dystonia

(a) (b)

Torticollis Torticaput Antecollis Retrocollis

Laterocollis Laterocaput
Antecaput Retrocaput

Fig. 2 a Collis and caput conditions (rotation and lateroflexion). b Collis and caput conditions (ante- and retroflexion)

triangle of the neck is highly variable. In some cases, the sternocleidomastoideus. It should be avoided when inject-
supraclavicular fossa is very deep and close to the ing muscles (Fig. 3).
pulmonary apex. In other cases, the region is fatty and Three prominent anatomic landmarks can be palpated on
the muscles can hardly be palpated. The external jugular the posterior aspect of the neck: the external occipital
vein passes through the triangle and crosses the protuberance (also called inion), the spinous process of C2
and the spinous process of C7. Between C2 and C7, the
spinous processes of C3, C4, C5 and C6 can sometimes be
palpated in thin patients. These three landmarks are of
value to define the vertebral levels and to guide the
injection. In a global manner, it is not recommended to
inject above the C2 level because of the risk of hitting the
vertebral artery (Fig. 4).
SC SCM

1 Cervical muscle dysfunctions


LS
The functions of a cervical muscle depend on the position
of the ‘‘head and neck complex’’. They are usually
T SM
described in healthy subjects in a neutral position of the
head and neck (Tabeke et al. 1974; Mayoux Benhamou
OH et al. 1997). In cervical dystonia, the cervical muscles act
on a ‘‘head and neck complex’’ that is in an abnormal, non-
2 physiological posture. As a consequence, the functions of
cervical muscles in cervical dystonia are sometimes not the
Fig. 3 Lateral cervical region. SCM sternocleidomastoideus muscle, physiological ones. Moreover, in cervical dystonia, the
SC splenius capitis muscle, LS levator scapulae muscle, SM scalenus
medius muscle, T trapezius muscle (pars descendens), OH Omohy- functions of a given muscle may be influenced by other
oideus muscle, 1 external jugular vein, 2 common carotid artery dystonic cervical muscles.

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L. Tatu, W. H. Jost

I
2
3
C2
1

C7

Fig. 5 Muscles involved in cervical dystonia. Example of right


lateroflexion. 1 Some of the right paravertebral muscles (splenius and
semispinalis muscles) may act as dystonic muscles, 2 left upper
trapezius muscle should be regarded as an ‘‘antagonist’’ muscle,
passively tensed by the abnormal movement, 3 right levator scapulae
muscle is a compensatory muscle. Right shoulder elevation helps
patient to correct his gaze
Fig. 4 Posterior cervical region. I inion (external occipital protuber-
ance), C2 C2 spinous process, C7 C7 spinous process. Red zone risk
of hitting vertebral artery, orange zone risk of hitting pulmonary apex, Cervical dystonia is a global disease inducing hyperac-
green zone no major risk. Blue spots injection sites tivity, spasms, tremor in a good number of cervical mus-
cles. Obviously, it is not possible to treat all the hyperactive
From a semiologic point of view, cervical muscles muscles with botulinum toxin. We know that a few muscles
involved in cervical dystonia can be divided according to are more frequently involved and may be the leading
two main classifications. First, considering their insertions, muscles. They, therefore, have to be injected first. These
cervical muscles can be classified into muscles acting key muscles may also be specifically activated during
mainly on the head or mainly on the neck. This distinction certain tasks, such as walking, sitting or closing eyes. They
corresponds to the anatomical basics of the ‘‘collis caput may explain transient worsening of cervical dystonia dur-
complex’’. This approach is very useful to select the ing these tasks.
muscles to be injected with botulinum toxin. As an For decades, splenius capitis and sternocleidomas-
example, the sternocleidomastoideus muscle, inserted on toideus have been considered as the key muscles involved
the mastoid process, is only able to act on the head, and the in cervical dystonia and the main targets of botulinum toxin
semispinalis cervicis muscle, inserted on the cervico-tho- injections. The choice of these muscles, both inserted on
racic spine, can only exercise action on the neck. the head, was guided by their involvement in rotation in
Second, cervical muscles can also be classified in three physiological conditions. Sternocleidomastoideus, as the
groups: dystonic, ‘‘antagonist’’ and ‘‘compensatory’’, most obvious muscle of the region, became an overused
depending on their type of involvement in cervical dys- and over-injected muscle in cases of rotation in cervical
tonia. Dystonic muscles are able to induce abnormal dystonia. In fact, sternocleidomastoideus, such as splenius
movement, posture or spasms. Hyperactivity can be capitis, are inserted on the head and not on the neck. So, in
recorded in these muscles with electromyography, and cervical dystonia, if the head is not mainly concerned by
they are mainly the target of botulinum toxin therapy. The the abnormal movement, they are only weakly involved.
‘‘antagonist’’ muscles are passively tensed by abnormal Taking into account the new semiologic approaches and
movement or posture. They can sometimes act as real the deep cervical muscles, more frequently used as a target
antagonist muscles inducing opposite movements or tre- for botulinum toxin in cervical dystonia, new key muscles
mor. In rare cases, they should also be injected. The have to be considered: e.g., levator scapulae and obliquus
‘‘compensatory’’ muscles may help the patients to correct capitis inferior. These ‘‘non-conventional’’ muscles should
their posture and their gaze. As they act as useful muscles have a stronger role in today’s botulinum toxin therapy.
for the patients, they should not be treated by botulinum Obviously, further clinical studies are needed to define the
toxin (Fig. 5). Moreover, any compensation can mask an priorities for the use of these muscles.
abnormal movement. For example, shoulder elevation can Levator scapulae acts mainly on the neck inducing a
limit lateroflexion of the head and neck. During clinical homolateral rotation and lateroflexion. In physiological
examination, if the shoulder is fixed, then the abnormal conditions, participation of levator scapulae in head and
movement becomes obvious. neck motion has been considered as negligible (Bull et al.

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Anatomy and cervical dystonia

1984; Mayoux Benhamou et al. 1995). Obliquus capitis


inferior is the biggest suboccipital muscle acting as an
important homolateral rotator of the head in cervical dys-
tonia (Schramm et al. 2014). In physiological conditions,
obliquus capitis inferior is regarded as a powerless rotator
muscle (Kapandji 2008).

A new interest for the deepest layer


of the posterior cervical muscles

Cervical muscles are classified according to their positions


around the cervical spine. The anterior group includes the
platysma and the deep prevertebral muscles: longus capitis
and longus colli muscles. They are mainly involved in the
flexion of the head but are difficult to inject with botulinum
toxin in daily practice (Hefter et al. 2012). The lateral
group includes sternocleidomastoideus, levator scapulae
and scalenus muscles, all inserted on the pectoral girdle.
They are easier to inject using cervical anatomical land-
marks of the lateral part of the neck.
Anatomic organization of posterior cervical muscles is
complex. For some authors, dorsal neck muscles consist of Fig. 6 Deep posterior cervical muscles. 1 Inion (external occipital
protuberance), 2 C2 spinous process, 3 C7 spinous process, 4 obliquus
four muscular layers (Mayoux Benhamou et al. 1997; capitis inferior muscle, 5 semispinalis cervicis muscle
Kapandji 2008). From a practical point of view, it seems
more accurate to consider the posterior cervical muscles as
organized in three layers (superficial, middle and deep). more frequently used in treatment procedures. Injecting
The superficial layer is formed by the upper trapezius toxin in obliquus capitis inferior or semispinalis cervicis
muscle and the middle layer by the splenius capitis, sple- muscle can be helpful in different types of cervical
nius cervicis, longissimus capitis, longissimus cervicis and dystonia.
semispinalis capitis muscles. The deep layer includes the Ultrasonography is the most accurate guidance to inject
suboccipital muscles, the semispinalis cervicis and multi- a given muscle of these posterior muscles. For example, it
fidus muscles. All of these muscles, except the upper allows us to inject selectively splenius capitis muscle or
trapezius and the suboccipital muscles, are organized in the semispinalis capitis muscle in the middle layer and to reach
same way: a common paravertebral lower insertion that safely obliquus capitis inferior in the deepest layer
gives rise to two components: one to the head and one to (Schramm et al. 2015).
the neck. A fatty layer, including numerous veins, is
inserted between the deep and the middle muscular layers.
When injecting botulinum toxin, hitting a vein in this layer The importance of the architecture of cervical
may lead to bleeding and to post-injection pain. muscles
In the last decade, new attention has been paid to the
deepest muscular layer, which can be divided into two Muscle architecture definition includes: anatomy of tendi-
levels. The upper one (above C2 level) includes four short nous parts of the muscles, muscular organization and
suboccipital muscles (rectus capitis major and minor neuromuscular compartments and, as a consequence,
muscles, obliquus capitis superior and inferior muscles). location of neuromuscular junctions. These data are rarely
The lower one (below C2 level) is made of two muscles: taken into account in treating cervical dystonia with
the semispinalis cervicis muscle lying on the multifidus botulinum toxin.
muscle. Obliquus capitis inferior appears as a powerful Cervical muscles, as numerous other muscles, are
homolateral rotator of the head in cervical dystonia. The organized around tendinous parts or include large or long
semispinalis cervicis muscle is involved in the homolateral tendons. The architecture of a given muscle is the major
rotation of the neck (Fig. 6). determinant of its function. The main components of this
These deepest muscles of the neck, sometimes consid- architecture are muscle fibers, which are inserted on
ered as too difficult to inject with botulinum toxin, are now intramuscular fibrous structures. The latter form a

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L. Tatu, W. H. Jost

connective tissue network, a ‘‘fibrous skeleton’’ of muscle, zones can also be approached by 3D surface electromyog-
including intramuscular aponeuroses that then densen into raphy (Falla et al. 2002; Delnooz et al. 2014). Using this
tendons inserted on the bone (Tatu and Parratte 2016). method in a recent study, this zone was defined at the lower
Tendinous parts are to be avoided when injecting toxin. border of the superior third part of the sternocleidomas-
They usually participate in dividing the muscle into neu- toideus muscle and at half muscle length of the splenius
romuscular compartments, corresponding to separate capitis muscle (Delnooz et al. 2014). Obviously, this kind of
functional subunits formed of morphologically and func- elaborate process cannot be used in clinical practice.
tionally identical muscle fibers. Each compartment is Moreover, further studies are needed before implementing
innervated by an individual nerve branch and controlled by data on motor endplates locations in routine botulinum
a specific spinal neuronal population (Windhorst et al. toxin therapy.
1989; Segal et al. 1991). Nevertheless, most of the cervical
muscles’ compartments have to be described. Some of
them are known and sometimes visible in magnetic reso- Conclusion
nance imaging as in the case of semispinalis capitis muscle.
At least two compartments can be defined in this muscle: a Knowledge of topographic and functional anatomy of
vertical medial part, traversed by the great occipital nerve cervical muscles and cervical spine is an essential prereq-
at the C2–C3 level, and a lateral part, semi-circular in uisite for treating cervical dystonia patients with botulinum
shape. A global unilateral contraction of this muscle toxin. Recent insights have modified the conventional
induces homolateral rotation and lateroflexion and partic- anatomical conception of the head and neck complex.
ipates in the retroflexion of the head. Nevertheless, owing Moreover, some physiological and anatomic data are not
to its insertions, each compartment is involved differently accurate in cervical dystonia, a highly non-physiological
in these functions. condition. In this review, we have tried to focus on the
In some cases, ultrasonography allows us to specify more important practical anatomical points that should be
muscle organization such as in the case of levator scapulae taken into account to improve botulinum toxin efficiency in
muscle. This muscle is organized in four bundles inserted cervical dystonia.
onto the transverse processes of C1, C2, C3 and C4. These
bundles are visible in ultrasonographic images and can be
injected selectively with botulinum toxin to act on a given
vertebral level. The larger part of the muscle, where the References
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