Muscular Arrangement and Muscle Attachment Sites in the Cervical Region of the American Barn Owl (Tyto furcata pratincola)

Owls have the largest head rotation capability amongst vertebrates. Anatomical knowledge of the cervical region is needed to understand the mechanics of these extreme head movements. While data on the morphology of the cervical vertebrae of the barn owl have been provided, this study is aimed to provide an extensive description of the muscle arrangement and the attachment sites of the muscles on the owl's head-neck region. The major cervical muscles were identified by gross dissection of cadavers of the American barn owl (Tyto furcata pratincola), and their origin, courses, and insertion were traced. In the head-neck region nine superficial larger cervical muscles of the craniocervical, dorsal and ventral subsystems were selected for analysis, and the muscle attachment sites were illustrated in digital models of the skull and cervical vertebrae of the same species as well as visualised in a two-dimensional sketch. In addition, fibre orientation and lengths of the muscles and the nature (fleshy or tendinous) of the attachment sites were determined. Myological data from this study were combined with osteological data of the same species. This improved the anatomical description of the cervical region of this species. The myological description provided in this study is to our best knowledge the most detailed documentation of the cervical muscles in a strigiform species presented so far. Our results show useful information for researchers in the field of functional anatomy, biomechanical modelling and for evolutionary and comparative studies

M. longus colli dorsalis, pars cranialis.

<p>A) Dorsal view on M. longus colli dorsalis, pars cranialis. Vertebrae numbers are indicated (C2-C7). The slips from the pars cranialis insert to the tendo axialis (ta) from a pars caudalis (ca) slip. The lateral processus of C2, which serve as insertion point for the tendo axialis are indicated with broken lines. The M. interspinalis (is), M. splenius capitis (sc) and M. longus colli dorsalis, pars profunda (pr) are indicated for reference. Coordinate system indicates lateral (L), caudal (Ca) and cranial (Cr). Scale bar represents one centimetre. B-G) Muscle attachment sites of the M. longus colli dorsalis, pars cranialis indicated with red circles in the three-dimensional models of the vertebrae of <i>T</i>. <i>f</i>. <i>pratincola</i> from dorsal view (cranial is on top). Scale bars in B-G represent one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]). H) Connection diagram from lateral view of M. longus colli dorsalis, pars cranialis in <i>T</i>. <i>f</i>. <i>pratincola</i>; origin and insertion sites are connected with lines representing the muscle slips, broken lines represent the tendo axialis. The arrowhead indicates that this muscle slip (from the M. longus colli dorsalis, pars caudalis) runs further caudally. I) Connection diagram from dorsal view of M. rectus capitis ventralis in which the muscle attachment sites are indicated with red circles and are interconnected by a line representing the muscle slips. Broken lines indicate the tendo axialis. The arrowheads indicate that this muscle slip (from the M. longus colli dorsalis, pars caudalis) runs further caudally.</p

M. longus colli ventralis.

<p>A) Lateral view on M. longus colli ventralis. The muscle originates from T2 as indicated by an asterisk. Muscle starts fleshy and becomes aponeurotic and splits when it runs cranially. The aponeurotic parts can clearly be seen in the middle region. Coordinate system indicates dorsal (D), caudal (Ca), ventral (V) and cranial (Cr). Scale bar represents one centimetre. B-I) Muscle attachment sites of the M. longus colli ventralis indicated with red circles in the three-dimensional models of the vertebrae of <i>T</i>. <i>f</i>. <i>pratincola</i>: lateral left view (cranial is to the left). Scale bars represent one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]). J) Connection diagram from lateral view of M. longus colli ventralis in <i>T</i>. <i>f</i>. <i>pratincola</i>; origin and insertion sites are connected with lines representing the muscle slips, broken lines represent aponeurotic parts. K) Connection diagram from dorsal view of M. rectus capitis ventralis in which the muscle attachment sites are indicated with red circles and are interconnected by lines representing the muscle slips. The blue lines represent ventrally located slips, which are thus actually behind the field of vision in a dorsal view.</p

M. longus colli dorsalis, pars cranialis.

<p>A) Dorsal view on M. longus colli dorsalis, pars cranialis. Vertebrae numbers are indicated (C2-C7). The slips from the pars cranialis insert to the tendo axialis (ta) from a pars caudalis (ca) slip. The lateral processus of C2, which serve as insertion point for the tendo axialis are indicated with broken lines. The M. interspinalis (is), M. splenius capitis (sc) and M. longus colli dorsalis, pars profunda (pr) are indicated for reference. Coordinate system indicates lateral (L), caudal (Ca) and cranial (Cr). Scale bar represents one centimetre. B-G) Muscle attachment sites of the M. longus colli dorsalis, pars cranialis indicated with red circles in the three-dimensional models of the vertebrae of <i>T</i>. <i>f</i>. <i>pratincola</i> from dorsal view (cranial is on top). Scale bars in B-G represent one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]). H) Connection diagram from lateral view of M. longus colli dorsalis, pars cranialis in <i>T</i>. <i>f</i>. <i>pratincola</i>; origin and insertion sites are connected with lines representing the muscle slips, broken lines represent the tendo axialis. The arrowhead indicates that this muscle slip (from the M. longus colli dorsalis, pars caudalis) runs further caudally. I) Connection diagram from dorsal view of M. rectus capitis ventralis in which the muscle attachment sites are indicated with red circles and are interconnected by a line representing the muscle slips. Broken lines indicate the tendo axialis. The arrowheads indicate that this muscle slip (from the M. longus colli dorsalis, pars caudalis) runs further caudally.</p

M. rectus capitis lateralis.

<p>A) Dorsolateral view on the M. rectus capitis lateralis (rcl). The muscle originates ventrally from C3-C5 (indicated by asterisks), wraps around the neck and inserts on the cranium. The M. rectus capitis lateralis is located superficially from the M. splenius capitis (sc) and M. rectus capitis dorsalis (rcd). Coordinate system indicates ventral (V), cranial (Cr), dorsal (D) and caudal (Ca). Scale bar represents one centimetre. B) Connection diagram from lateral view of M. rectus capitis lateralis in <i>T</i>. <i>f</i>. <i>pratincola</i>; origin and insertion sites are connected with lines representing the muscle slips, broken lines indicate tendinous parts. C) Connection diagram from dorsal view of M. rectus capitis lateralis in which the muscle attachment sites are indicated with red circles and are interconnected by a line representing the muscle slips. The blue lines represent ventrally located slips, which are thus actually behind the field of vision in a dorsal view. D) Dorsal view on the skull with indicated insertion sites of the M. rectus capitis lateralis. Foramen magnum (FM) and condylus occipitalis (CO) are indicated. Scale bar represents one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]). E-G) Origins of the M. rectus capitis lateralis indicated with red ellipses in the three-dimensional models of the vertebrae of <i>T</i>. <i>f</i>. <i>pratincola</i> from ventral view (cranial is on top) of vertebrae (C3-C5). Scale bars in E-G represent one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]).</p

M. rectus capitis ventralis.

<p>A) Craniocervical region from ventral view showing the M. rectus capitis ventralis from which the M. rectus capitis ventralis sinister, pars lateralis (l) and pars medialis (m) are bordered by a broken line. Coordinate system indicates lateral (L), caudal (Ca) and cranial (Cr). Scale bar represents one centimetre. B) Skull from caudal view with indicated foramen magnum (FM) and insertion site of M. rectus capitis ventralis on the os basioccipitale (red line). Scale bar represents one millimetre. C-G) Muscle attachment sites of the M. rectus capitis ventralis indicated with red ellipses in the three-dimensional models of the vertebrae of <i>T</i>. <i>f</i>. <i>pratincola</i>: ventral view (cranial is on top). Scale bars in C-G represent one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]). H) Connection diagram from lateral view of M. rectus capitis ventralis in <i>T</i>. <i>f</i>. <i>pratincola</i>; origin and insertion sites are connected with lines representing the muscle slips. I) Connection diagram from dorsal view of M. rectus capitis ventralis in which the muscle attachment sites are indicated with red circles and are interconnected by a line representing the muscle slips.</p

Myology of <i>T</i>. <i>f</i>. <i>pratincola</i> indicated in a semi-diagrammatic reconstruction of the S-shaped neck.

<p>Reconstruction of the back of the skull, the 14 cervical vertebrae and the first thoracic vertebra, the second thoracic vertebra is represented diagrammatically, because a three-dimensional model was lacking. The vertebrae are positioned in a natural S-shape which is based on X-ray images made from <i>T</i>. <i>f</i>. <i>pratincola</i> in rest [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]. The numbers in the cervical vertebrae represent the osteological regions as defined by Krings et al. (2014) [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]. Osteological regions were defined as follows; region 1: C1, region 2: C2-C4, region 3: C5-C7, region 4: C8-C9, region 5: C10-C12 and region 6: C13-C14 [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]. Fleshy parts are indicated with solid lines, broken lines represent tendinous or aponeurotic parts. The heavy lines above C14, T1 and T2 represent the aponeurosis notarii. Colours are given for clarity and represent the individual muscles as listed below. Dorsally originating muscles: M. complexus (red), M. biventer cervicis (black), M. splenius capitis (purple), M. rectus capitis dorsalis (blue), M. longus colli dorsalis, pars caudalis (pink), M. longus colli dorsalis, pars cranialis (yellow), pars profunda (green), M. interspinalis (orange). Ventrally originating muscles: M. rectus capitis lateralis (yellow), M. rectus capitis ventralis (red), M. longus colli ventralis (black). Note that this figure represents an overview of the relative muscle positions. This figure does not represent precise attachment sites. These were already provided in Figs <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.g001" target="_blank">1</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.g012" target="_blank">12</a>.</p

Connection diagram of the cervical muscles as identified in <i>T</i>. <i>f</i>. <i>pratincola</i> from lateral view.

<p>The head is represented as a rectangle and the fourteen cervical vertebrae and the first two thoracic vertebrae are represented as squares. The cervical vertebrae are numbered, and the consecutive numbers of the same region as defined by Krings et al. (2014) [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>] are represented by the alternating use of bold and italic numbers. Osteological regions were defined as follows; region 1: C1, region 2: C2-C4, region 3: C5-C7, region 4: C8-C9, region 5: C10-C12 and region 6: C13-C14 [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]. The thoracic vertebrae were excluded from the regionalization [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]. Fleshy parts are indicated with solid lines; broken lines represent tendinous or aponeurotic parts. The heavy lines above C14, T1 and T2 represents the aponeurosis notarii. Colours are given for clarity and represent the individual muscles as listed below. Dorsally originating muscles: M. complexus (red), M. biventer cervicis (black), M. splenius capitis (purple), M. rectus capitis dorsalis (blue), M. longus colli dorsalis, pars caudalis (pink), M. longus colli dorsalis, pars cranialis (yellow), pars profunda (green), M. interspinalis (orange). Ventrally originating muscles: M. rectus capitis lateralis (yellow), M. rectus capitis ventralis (red), M. longus colli ventralis (black). Note that this figure represents an overview of the relative muscle positions. This figure does not represent precise attachment sites. These were already provided in Figs <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.g001" target="_blank">1</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.g012" target="_blank">12</a>.</p

M. interspinalis.

<p>A) Dorsal view on M. interspinalis (is) spanning the space between the processus spinosus of C2 (insertion) and C3 (origin) which are indicated by asterisks whereas the tori dorsales of C2 are indicated by circles with broken lines. The M. splenius capitis (sc), M. longus colli dorsalis, pars cranialis (cr) and a slip from the M. longus colli dorsalis, pars caudalis (ca) are indicated as a reference. Coordinate system indicates lateral (L), caudal (Ca) and cranial (Cr). Scale bar represents one centimetre. B-C) Muscle attachment sites of the M. interspinalis indicated with red circles in the three-dimensional models of the vertebrae of <i>T</i>. <i>f</i>. <i>pratincola</i>: lateral view (cranial is to the left). Scale bars represent one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]). D) Connection diagram from lateral view of the M. interspinalis origin and insertion sites are connected with a line representing the muscle. E) Connection diagram from dorsal view of M. interspinalis in which the muscle attachment sites are indicated with red circles and are interconnected by a line representing the muscle.</p

M. complexus.

<p>A) Dorsolateral view of M. complexus sinister (c) held up with tweezers; fleshy insertion site on the cranium (cr) and originating muscle slips from cervical vertebrae C4-C6 are indicated by asterisks. The M. splenius capitis (sc) and M. rectus capitis lateralis (rcl) are indicated as a reference. The coordinate system indicates dorsal (D), caudal (Ca), ventral (V) and cranial (Cr). Scale bar represents one centimetre. B) Dorsal view on both M. complexus sinister and dexter (c) showing variation between the sides. The insertion of the M. complexus dexter was separated from the cranium (cr). Individual slips (attaching to C4-C6) are indicated by asterisks. The M. complexus sinister has an extra slip originating from C3. The coordinate system indicates lateral (L), caudal (Ca) and cranial (Cr). Scale bar represents one centimetre. C) Insertion site of M. complexus indicated with red line in three-dimensional model of a part of the skull from dorsal view. Foramen magnum (FM) and condylus occipitalis (CO) are indicated. Scale bar represents one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]). D-F) Origins of the M. complexus indicated with red circles in the three-dimensional models of the vertebrae of <i>T</i>. <i>f</i>. <i>pratincola</i>; vertebrae (C4-C6) from lateral left view, cranial is to the left. Scale bars in D-F represent one millimetre (adapted from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0134272#pone.0134272.ref005" target="_blank">5</a>]). G) Connection diagram from lateral view of M. complexus in <i>T</i>. <i>f</i>. <i>pratincola</i>; origin and insertion sites are connected with lines representing the muscle slips. H) Connection diagram from dorsal view of M. complexus in which the muscle attachment sites are indicated with red circles and are interconnected by a line representing the muscle.</p