- Research article
- Open Access
Digital dissection of the head of the rock dove (Columba livia) using contrast-enhanced computed tomography
© The Author(s). 2019
- Received: 10 January 2019
- Accepted: 9 April 2019
- Published: 10 June 2019
The rock dove (or common pigeon), Columba livia, is an important model organism in biological studies, including research focusing on head muscle anatomy, feeding kinematics, and cranial kinesis. However, no integrated computer-based biomechanical model of the pigeon head has yet been attempted. As an initial step towards achieving this goal, we present the first three-dimensional digital dissection of the pigeon head based on a contrast-enhanced computed tomographic dataset achieved using iodine potassium iodide as a staining agent. Our datasets enable us to visualize the skeletal and muscular anatomy, brain and cranial nerves, and major sense organs of the pigeon, including very small and fragile features, as well as maintaining the three-dimensional topology of anatomical structures. This work updates and supplements earlier anatomical work on this widely used laboratory organism. We resolve several key points of disagreement arising from previous descriptions of pigeon anatomy, including the precise arrangement of the external adductor muscles and their relationship to the posterior adductor. Examination of the eye muscles highlights differences between avian taxa and shows that pigeon eye muscles are more similar to those of a tinamou than they are to those of a house sparrow. Furthermore, we present our three-dimensional data as publicly accessible files for further research and education purposes. Digital dissection permits exceptional visualisation and will be a valuable resource for further investigations into the head anatomy of other bird species, as well as efforts to reconstruct soft tissues in fossil archosaurs.
- Jaw muscles
- Eye muscles
- Hyolingual apparatus
- Digital dissection
The rock dove (Columba livia), also known as the common or domestic pigeon, is one of the most abundant, widely distributed, and morphologically disparate bird species, including over 350 breeds [1, 2], and has a long association with human culture . Careful documentation of variations in rock dove morphology and behaviour were key to the development of evolutionary theory  and, more recently, it has become an important model organism in biological sciences, including genetics [5, 6], evolutionary biology [1, 2, 6–8], neuroscience and behaviour [9–13], vision , biomimetics , developmental biology , medicine [17, 18] and biomechanics [19, 20], including feeding studies [21–29].
Previous descriptions of jaw, neck, and throat muscles in columbiform birds
Marquesan ground dove
Burton 1974 
Bhattacharyya 2013 
Nicobar green imperial pigeon
Bhattacharyya 1994 
Hodgson’s imperial pigeon
Bhattacharyya 1994 
Indian spotted dove
Bhattacharyya 1994 
Bhattacharyya 1994 
Bruce’s green pigeon
Burton 1974 
common green pigeon
Merz 1963 
Merz 1963 
Merz 1963 
Advances in medical imaging and computing power have re-energized interest in vertebrate anatomy and facilitated the creation of three-dimensional (3D) digital anatomical and biomechanical models (e.g. [47–59]). Over the past decade, foundational information from gross dissection has been built on by an increasing number of ‘digital dissections’ using radiographic contrast agents, particularly iodine potassium iodide (I2KI) combined with high-resolution micro-computed tomographic (μCT) scanning [60–62], widely known as diffusible iodine-based contrast-enhanced μCT, or diceCT . Unlike gross dissection, diceCT is non-destructive, permits visualization of very small and fragile specimens, and preserves the 3D topology of anatomical structures. Furthermore, digital dissections produced through diceCT can be used to create interactive 3D reconstructions for wider distribution to the public, students, and researchers. Digital dissections have been produced for a range of vertebrates, including fish , amphibians , non-avian reptiles [66–68], and mammals [69–72], as well as various anatomical regions of some birds [58, 73, 74]. Digital dissections have also been possible with unenhanced μCT [75, 76], magnetic resonance imaging , and histological sections .
Here, we provide the first 3D digital dissection of the head of C. livia and a critical synthesis of previous anatomical descriptions of this model organism. We focus on musculoskeletal anatomy, although our work also covers some aspects of the cranial nerves, glands, and eye. In particular, we use these data in an attempt to resolve discrepancies between earlier anatomical descriptions, providing a crucial first step towards developing a three-dimensional biomechanical model of the pigeon skull. These data will also assist reconstructions of head muscles in non-model birds, as well as contributing to a broader understanding of archosaur jaw muscle evolution ([58, 75, 79–85].
A deceased and previously frozen adult specimen of Columba livia with a body mass of 242 g was obtained from Jim Usherwood and John Hutchinson (Royal Veterinary College, Hatfield, UK).
Columba livia is an anatomically disparate species that includes 350 breeds  classified within the clade Columbiformes, which contains approximately 44 genera and 315 species of pigeons and doves . According to analyses of nDNA Columbiformes is the sister taxon to a clade comprising Pteroclidiformes (sandgrouses) + Mesitornighiformes (mesites) [87, 88]. Together, these clades form the Columbimorphae, within the larger group Neoaves [87, 88]. Genome scale analyses place the origin of crown group Columbiformes between 18.9 and 31.3 Ma, within the Oligocene or earliest Miocene .
The specimen was CT scanned three times in 2016 at the Cambridge Biotomography Centre (Zoology Department, University of Cambridge): once prior to staining, once after staining, and once after some staining was removed. All scans were performed with a Nikon X-Tek H 225 μCT scanner (Nikon Metrology, Tring, UK) and used a tungsten target, a background medium of air, no filter, and were rendered as 16-bit TIFFs. The first scan, prior to staining, used settings of 80 kV and 230 μA, exposure 1000 ms, 720 projections, and no frame averaging to produce 1946 TIFF slices at 0.113 mm/voxel. The second scan was made after staining. The head was severed between the third and fourth cervical vertebrae and fixed in 4% phosphate-buffered paraformaldehyde solution. It was stained in a solution of 7.5% weight-by-volume I2KI for 11 days; the solution was neither refreshed nor agitated during this time. This second scan used settings of 140 kV and 90 μA, exposure 1000 ms, 720 projections, and no frame averaging to produce 1267 TIFF slices at 0.0397 mm/voxel. The third scan took place after some of the stain was removed using three separate changes of ethanol and settings of 120 kV and 250 μA, exposure 500 ms, 3141 projections, no frame averaging, to produce 1603 TIFF slices at of 0.0303 mm/voxel.
Three-dimensional surfaces were smoothed (Additional file 4) and exported as wavefront (OBJ) files to create interactive 3D PDFs using Tetra4D Reviewer and Converter (Tech Soft 3D, Oregon, USA) and Adobe Acrobat Pro X (Adobe Systems, California, USA) following previous studies [92, 93]. The smoothing was necessary due to file size constraints. These digital models are provided as supporting information (Additional file 1), and are the basis for the following description.
Abbreviations used throughout the figures and manuscript text. Bones are in all uppercase. Muscles and glands are in title case following a lower case m or g, ligaments are in title case following a capital L, and specific features are all lowercase with abbreviations separated by a full stop
Aponeurosis of the mAMEM
ophthalmic division of the trigeminal nerve
maxillary division of the trigeminal nerve
mandibular division of the trigeminal nerve
crista posterolateral palatinus
foramen for the vagus nerve
foramen for the hypoglossal nerve
foramen for the occipital vein
ligament 2, ligamentum Occipitomandibule
ligament 5, ligamentum Postorbital
ligament 6, ligamentum Quadratomandibular
musculus Adductor Mandibulae Externus pars Medialis
musculus Adductor Mandibulae Externus pars Medialis portion a
musculus Adductor Mandibulae Externus pars Medialis portion b
musculus Adductor Mandibulae Externus pars Profundis
musculus Adductor Mandibulae Externus pars Superficialis
musculus Adductor Mandibulae Posterior
musculus Biventer Cervicis
musculus Depressor Mandubulae
musculus Flexor Colli
musculus Genioglossus Anterior
musculus Hypoglossus Obliquus
musculus Hypoglossus Rectus
musculus Levator Palpebrae Dorsalis
musculus Levator Palpebrae Ventralis
musculus Obliquus Dorsalis
musculus Obliquus Ventralis
musculus Protractor Pterygoidei et Quadrati
musculus Pseudotemporalis Profundus
musculus Pseudotemporalis Superficialis
musculus Pterygoideus Dorsalis Anterior
musculus Pterygoideus Dorsalis Medialis
musculus Pterygoideus Dorsalis Posterior
musculus Pterygoideus Ventralis
musculus Pyramidalis Membrane Nictitans Ligament
musculus Pyramidalis Membrane Nictitans
musculus Quadratus Membrane Nictitans
musculus Rectus Capitis Ventralis
musculus Rectus Capitis Dorsalis
musculus Rectus Capitis Lateralis
musculus Rectus Dorsalis
musculus Rectus Lateralis
musculus Rectus Medialis
musculus Rectus Ventralia
musculus Splenius Capitis Medialis
musculus Splenius Capitis Lateralis
Previous descriptions of columbiform skulls include those of Rooth  Ghetie  Bhattacharyya  van Gennip  Burton , and two of these studies [30, 33] include descriptions of Columba livia.
Each lower jaw comprises six bones (dentary, splenial, surangular, prearticular, articular, and angular) but all except the dentary are fused in adults, such that individual sutures are not visible . Both rami are also fused at the symphysis. In lateral view the anterior half of the lower jaw is at a 30° angle to the long-axis of the posterior half. The posterior surface is flat and triangular (Fig. 3b).
In birds the hyoid skeleton (hyobranchialis apparatus, Additional file 2) comprises three midline elements and a pair of long thin structures (the cornu branchiale) that arise from the junction between the two posterior midline elements (Fig. 3b; [32, 36, 96]). The anterior-most midline element is the cartilagenous paraglossum (=entoglossum). In contrast to some species, the paraglossum in C. livia is unpaired (but see ). It has an arrowhead-like shape in dorsal view due to the posterolaterally projecting cornua (Fig. 2b; ). Its anterior surface is relatively smooth whereas the posterior end bears small spines. The cornified outer ventral layer and tough (but elastic) dorsal layer (described in Bhattacharyya ) are both visible in our CT data. The central midline element is the basihyale (=basibranchiale rostrale) and the posterior midline element is the urohyale (=basibranchiale caudale). Both the basihyale and urohyale are flat. Each cornu branchiale comprises a proximal ceratobranchiale, a more distal epibranchiale (=ceratobranchiale II), and in some species a further distal pharyngobranchiale (Fig. 3b; ). The latter is present but unossified in C. livia and discernible in the CT slices due to the surrounding tissues. Birds exhibit great morphological disparity in the relative proportions of the hyoid skeleton with differences reflecting phylogeny and mode of feeding . The hyoid skeleton of C. livia has a rather short basihyale and very long gracile cornua [32, 36]. The paraglossum articulates with the convex anterior surface of the basihyale .
The skull ligaments of columbiform birds  (van Gennip 1986)
tip of the palatine
restricts dorsal movement of the maxilla
posterodorsal edge of the lower jaw
restricts movements of the lower jaw
restricts medial movements of the lower jaw
posteromedial side of the quadrate
restricts lateral and dorsal directed movements of the quadrate relative to the cranium
facilitates kinesis of the upper jaw
lateral side of the lower jaw
restricts rostral and medial movements of the quadrate relative to the lower jaw
dorsal surface of the lower jaw
restricts lateral movements of the quadrate relative to the lower jaw
restricts movement of the jugal arch away from the prefrontal
It may also restrict anteroventral movement of the lower jaw (locking it) until contraction of the m. Protractor Pterygoidei et Quadrati rotates the quadrate forwards [26, 27, 29, 33, 95, 103]. The ligamentum quadratomandibular (L6) is short and closely associated with the L5. It spans between the quadrate and lower jaw and is situated just anterior to the jaw joint. This ligament restricts anterior and medial movements of the lower jaw relative to the quadrate . Ligamentous tissue is also present between the ventral and lateral edges of the occipital condyle and the corresponding edge of the atlas (LOccAt). This tissue presumably supports the connection between the skull and neck, and in particular restricts dorsal and mediolateral movements of the head relative to the atlas. A further possible ligament (LDenBran) is visible originating from the posteromedial corner of the lower jaw between the insertion of the m. Pterygoideus Ventralis and m. Depressor Mandibulae. It passes ventrally and folds under the hyoid apparatus, which it presumably supports. This structure does not seem to have been previously described in the literature and it is located posterior to the detailed histological slices presented by Zweers .
m. Adductor Mandibulae Externus (m. AME)
m. Adductor Mandibulae Externus pars Superficialis (m. AMES)
Path: It passes anteroventrally for only a few millimetres before converging on a point that likely corresponds to the end of an aponeurosis (Figs. 7d, 8c). Ventrally it is bounded by the m. Adductor Mandibulae Externus pars Medialis.
m. Adductor Mandibulae Externus pars Medialis (m. AMEM)
The m. Adductor Mandibulae Externus pars Medialis lies ventrolateral to the m. AMES (Figs. 6, 7e, 8, 9d; [30, 33]). This peripheral origin and lateral insertion on the lower jaw suggests a potential homology with the m. AMES of lepidosaurs and turtles [47, 76, 97]. Internally the muscle includes a space that likely corresponds to a prominent aponeurosis (Fig. 7c; Additional file 1) . It extends from near the origin, giving the muscle a pennate structure (Fig. 9b) and allows it to be further divided into an anterior (m. AMEMa) and posterior portion (m. AMEMb).
Origin: Three short aponeuroses: one originating from the postorbital process and two from the zygomatic process (Figs. 8a, 9d). This three-part origin is consistent with the description of van Gennip , rather than those by others [30, 38, 42], who only describe its origin from the processus zygomaticus (=temporalis).
Path: Both parts pass anterior ventrally lateral to the location of the m. Adductor Mandibulae Profundus and m. Pseudotermporalis profundis.
Function: Contraction of this muscle rotates the lower jaw upwards. It is particularly active between the stationing and transport phases of feeding  as well as the jaw-closing phase of drinking .
m. Adductor Mandibulae Externus pars Profundus (m. AMEP)
The medial boundary of the m. AMEP has been reported to be difficult to separate from the lateral portion of the m. Adductor Mandibulae Posterior [33, 105]. However, in our dataset this division can be discerned on both sides.
m. Adductor Mandibulae Posterior (m. AMP)
As mentioned above, we find the m. AMP to be reasonably distinct from the m. AMEP (contra ). It is also clearly separated from the m. Pseudotemporalis Profundus [33, 105] in contrast to the arrangement in Columba palumbus [39, 105].
Origin: The ventral part of the anterolateral surface of the quadrate (Fig. 8a) ventro medial to the origin of the mAMEP.
Function: Given its size and location, the m. AMP probably plays a role in stabilising the lower jaws during closure and possibly in jaw opening . Its in vivo activity has not been examined directly [27, 28].
m. Pseudotemporalis (m. Pst)
The m. Pseudotemporalis is part of the internal jaw adductor complex that lies medial to the lateral-most extent of CN V (Fig. 6; ). Within Sauropsida (e.g., [47, 76, 79]), it is often divided into superficial and deep muscles with separate origins and insertions. This is also the case in C. livia, but not in C. palumbus in which the two muscles merge [39, 105].
m. Pseudotemporalis Superficialis (m.PstS)
Path: Anteroventrally and converging anteriorly (Figs. 7a, 9g). In the CT dataset, CN V2 passes ventral to the main body of the segmented muscle. This is where the aponeurosis would be and therefore the location of the nerve is consistent.
m. Pseudotemporalis Profundus (m. PstP)
Variation in the size of this muscle (=m. quadratormandibularis in ) among columbiform birds has been linked to differences in beak length [33, 42]. It is situated medial to the pterygoid branch of CN V3 (sensu Bhattacharyya ) and m. AMP (Figs. 6, 7a, 9h; Additional file 1), whereas the main branch of CN V3 passes through it and into the Meckelian groove (Fig. 4).
Origin: A small region on the medialmost end of the medial process of the quadrate (Fig. 8a) medial to the mAMP.
Insertion: A broad area on the lateral, dorsal, and medial surfaces of the lower jaw anterior to the coronoid process; this insertion also includes the majority of the adductor fossa (8 c, d, 9 h; [33, 105]).
m. Pterygoideus (m. PT)
m. Pterygoideus Dorsalis (m. PtDo)
Origin: The anterior part (=rostralis of van Gennip ) originates from the dorsolateral surface of the palatine whereas the medial and posterior parts originate from the lateral surface of the pterygoid (Figs. 8a, 9i, 10). We do not observe any part of the anterior part originating from the pterygoid (contra Bhattacharyya ).
Insertion: The anterior part inserts posteroventral to the insertion of the m. PstP, via an aponeurosis  whereas the posterior and medial parts insert on the medial surface of the lower jaw between the insertion of the m. PstP and the point of jaw articulation, and posterodorsal to the insertion of the m. PtDoAn (Fig. 10a, b, c; Additional file 1).
Function: Contraction of these muscles closes the lower jaw and provides a significant supportive role against torsion or long axis bending of the jaws.
m. Pterygoideus Ventralis (m. PtVe)
Like the m. PtDo, the m. Pterygoideus ventralis in C. livia is often subdivided but there has been little consensus on the exact boundaries between these divisions in Columbiformes [33, 40, 42]. In our dataset, a division into two parts is incomplete and the lateral portion (referred to as the “venter externus” by Burton ), is not as large as that present in columbiform birds that eat fruit such as Didunculus [25, 31, 40].
Origin: The anterior-most part of the muscle originates from the posterolateral end of the ventral surface of the palatine whereas the posterior-most part originates from the ventral surface of the pterygoid (Figs. 6a, 9j; ).
Function: Contraction of the m. PtVe is particularly important for closing the jaws at large gapes. It is especially active during the grasping phase of feeding , but is also continuously active during drinking, with slightly greater activity during the jaw closing phase of drinking .
m. Protractor Pterygoidei et Quadrati (m. PPQ)
This muscle lies between the braincase and pterygoid-quadrate bar (Figs. 7, 9k) medial to CN V (Figs. 6, 7). As in lepidosaurs , some birds have two protractor muscles: one between the sphenoid and the pterygoid bones, and another from the sphenoid to the quadrate . However, in some other birds the two protractors are inseparable at their origin . Descriptions of this muscle in columbiform birds may refer to two separate muscles , but the majority report that there is no separation (e.g., [25, 30, 33, 38]). Our results are consistent with the latter interpretation although the origin has two distinct heads.
Origin: From the posterior surface of the orbit (Fig. 8a).
Path: The muscle divides into two heads. The posterior, dorsal-most head continues anterolaterally, whereas the anterior, ventral-most head passes more laterally (Fig. 9k).
Insertion: The dorsal-most head inserts on the dorsal edge and posterior surface of the anteromedial process of the quadrate whereas the ventral-most head inserts onto the posterior surface of the pterygoid (Fig. 8b).
Function: Contraction of this muscle facilitates protraction of the pterygo-quadrate-maxillopalatine complex and opening of the upper jaw [27, 31]. It is active during both the grasping and stationing phases of feeding  as well as the jaw closing phase of drinking . The frequent activity of the m. PPQ during feeding and the absence of variation associated with pellet size suggest that it has an important role in “unlocking” the kinetic mechanism .
m. Depressor Mandibulae (m. DM)
Insertion: On the lower jaw over a broad continuous area including its dorsolateral corner, the flat posterior surface of the lower jaw, and the posterior end of the medial surface (Figs. 6c, d and 11).
Function: This muscle primarily rotates the lower jaw; however, this muscle can also be involved in protraction of the upper jaw due to the mobility of the quadrate, postorbital ligament and action of other muscles such as the m. Protractor Pterygoidei et Quadrati [27, 95]. It is most active just prior to the gape, stationing, and intraoral transport phase of feeding , as well as the jaw opening phase of drinking . Its duration of activity is extended when dealing with particularly large food items .
Throat and tongue muscles
Previous descriptions of throat muscles in columbiform birds include those of Burk , Lubosch , Rawal , Burton , Bhattacharyya , and Zweers . Further useful descriptions of throat anatomy in birds include Engels  Harvey et al. , McLelland , George and Berger , Zusi and Storrer , and Huang et al. . Their sites of origin and insertion, as well as developmental history (based on the chicken Gallus gallus), can be used to divide the throat muscles into three groups: glossal, suprahyoid, and infrahyoid . Previous descriptions have used various synonyms for many of these muscles (Additional file 3). Here we mainly use the terminology of Bhattacharyya , and Huang et al. .
These muscles extend from the lower jaw to the hyobrachial skeleton . They are homologous to the suprahyoid muscles of mammals . They do not originate from somites and may derive from preoptic paraxial mesoderm [112, 113].
m. Mylohyoid (m. Mylo)
Origin: From the lingual edge of the dorsal ridge of the lower jaws (Fig. 12).
Path: It passes ventrally and medially (Fig. 12).
Function: Contraction of this muscle raises the floor of the mouth and reduces the volume of space within the oral cavity .
m. Serpihyoideus (m. Serp)
This muscle is spoon-shaped and composed of parallel fibres [30, 32]. Again an absence of muscle along the midline (Fig. 12) likely indicates the presence of the midline raphe . The m. Serpihyoideus lies anterior to, and continuous with, the m. Intermandibularis ventralis of Zweers  which is not described here.
Origin: On the posterodorsal surface of the lower jaw just posterior to the articular (Fig. 6d), posterior and lateral to the origin of the m. Stylohyoidues, and anterior to the insertion of the m. DM [30, 32].
Path: It passes anteromedially and superficial to the location of the urohyale (Fig. 12).
Function: This muscle serves to support the tongue and assist with raising the floor of the mouth .
m. Stylohyoideus (m. Styl)
This is a slender, strap-like muscle that is composed of parallel fibres, which lies deep to m. Serp and m. Mylo [30, 33]. In the CT dataset the m. Styl and m. Serp are difficult to separate from one another along the surface of the lower jaw.
Function: Contraction of this muscle results in retraction of the hyoid apparatus.
m. Branchiomandibularis (m. Bran)
This is a long muscle (=m. Branchiohyoideus of Li and Clarke ) that extends from the lower jaw to the cornu branchiale [30, 32]. There are two heads near to the point of origin that have been used as a basis for dividing the muscle into two parts [30, 32], but these separate heads are not obvious in our CT datasets.
Origin: From the lingual surface of the central part of the lower jaw (Fig. 12c) close to where the m. Styl passes ventral to the m. Mylo.
Path: It passes posteroventrally (in contrast to many of the other muscles in the throat) and passes deep to the m. Mylo, m. Serp, and m. Styl.
Function: Contraction of this muscle results in protraction of the hyoid apparatus. Greater development of this muscle in the columbiform birds Ducula and Treron supposedly allows greater tongue prehension for eating fruit .
m. Ceratohyoidues (m. Cerhy)
This is a strap-like muscle with parallel fibres [30, 32] located between the ceratobranchial and the posterior half of the urohyale. Although this contrasts with the more anterior location of the m. Cerhy in 10-day old chick embryos (: muscle 9), the location in adult chickens extends more posteriorly (: muscle f, see also ) and thus more closely resembles the arrangement observed in the pigeon, consistent with the inferred homology followed here.
Function: Contraction of this muscle would pull the cornu branchiale toward the midline or resist the m. Bran separating them.
These muscles, attached to the paraglossum, are homologous to the mammalian extrinsic lingual muscles and develop from somites 2–6 .
m. Genioglossus Anterior (m. GenglAn)
This is a thin muscle that extends along the floor of the mouth [30, 32]. Along with the m. GenglPo, it was referred to as the m. Sternomandibularis by Lubosch  and the m. Geniopharyngealis by .
Origin: Reportedly from near the symphysis of the lower jaw , but not clearly visible in CT datasets 2 or 3.
Path: Posteriorly parallel to the midline (Fig. 12b).
Function: Contraction of this muscle may have pulled the hyoid apparatus forwards. Greater development of this muscle in Ducula and Treron supposedly allows greater tongue prehension .
m. Genioglossus Posterior (m. GenglPo)
The posterior part is not clearly visible in any of our CT datasets , but it reportedly originates from the floor of the mouth on either side of the anterior end of the trachea , passes posteriorly parallel to the midline  and inserts near the posterior part of the cricoid cartilage .
m. Hypoglossus Rectus (m. HypRe)
Origin: From the ventral end of the paraglossum (Fig. 14a) near to its articulation with the basihyale and the insertion of the m. Ceratoglosssus (Fig. 12d). In chickens, the origin of this muscle may also involve the basihyale [109, 112].
Path: Anteriorly parallel to the midline (Fig. 12d).
Function: Contraction of this muscle results in flexion of the paraglossum.
m. Hypoglossus Obliquus (m. HypOb)
Path: The muscle passes dorsolaterally (Fig. 14a).
Function: Contraction of this muscle results in depression of the paraglossum .
m. Ceratoglossus (m. Cergl)
Path: This muscle passes anteroventrally along the lateral surface of the ceratobranchiale (Fig. 13c) deep to the m. Bran.
Function: Contraction of this muscle results in ventral and ventrolateral movement of the paraglossum .
These muscles extend from the larynx, tracheal cartilage, clavicle, and sternum to the hyobrachial skeleton and develop from somites 2–6 .
m. Cricohyoideus (m. Crico)
This muscle (= m. Thyrohyoideus of Bhattacharyya ) lies close to the midline. It originates on the ventral surface of the anterior end of the basihyal and inserts around the cricoid cartilage [30, 32].
Origin: This muscle originates from the posterior of the throat .
Path: It passes anteriorly parallel to the midline .
Insertion: Posterior end of the paraglossum and dorsal surface of the basihyale, dorsal to the insertion of the m. Styl (Fig. 14c).
Function: Contraction of this muscle retracts the hyoid apparatus.
m. Sternohyoides (m. Stern)
This is a strap-like muscle (= m. Claviculohyoideus of Zweers ).
Origin: This muscle originates from the sternum .
Path: It passes anteriorly lateral to the trachea and m. Crico .
Insertion: Posterior end of the paraglossum and dorsal surface of the basihyale (Fig. 14c), dorsal to the insertion of the m. Styl.
Function: Retraction of this muscle retracts the hyoid apparatus.
Morphological traits among the eye muscles of birds. Size comparisons for the rectus muscles are mainly based on their size at the point of insertion
Harvey et al. 1968
Chard and Gundlach 1937
Our digital segmentation
size of the mObDo relative to the mRecDo
twice as wide
twice as wide
size of m. RecLa vs mRecMe
location of the insertion of the mRecVe relative to the insertion of the mPyrMemNic
extent of overlap by the mRecVe of the origin of the mPyrMedNic
size of the mRecDo vs mRecVe
location of the insertion of the mObVe relative to the insertion of the mRecVe
extent of overlap by the mObVe of the origin of the mRecVe
proximity of the insertion of the mRecMe to the mObDo
Location of the insertion of the mRecDo relative to that of the mQuMemNic
aligned at lateral edges
aligned at lateral edges
aligned at medial edges
aligned at lateral edges
aligned at lateral edges
mRecMe > mRecLa
mRecMe > mRecDo
mRecMe > mRecVe
mRecDo > mRecVe
mRecDo > mRecLa
mRecLa > mRecVe
m. Palpebrae Obliquus (m. LevPalOb)
m. Quadratus Membrane Nictitans (m. QuMemNi)
As in all birds previously described, the m. Quadratus Membrane Nictitans is the larger of the two muscles associated with the nictitating membrane [58, 99, 100, 102]. It is innervated by CN VI .
Origin: A wide region of the dorsal part of the eye (Figs. 15a, 16f). It appears to be wider than in previous descriptions for the pigeon (Fig. 16d; ) which might reflect the difficulties in interpretations of where muscle ends and tendon begins.
Path: It covers a significant part of the medial surface of the eyeball converging towards CN II. In medial view it is partly obscured by the m. Rectus Dorsalis, m. Rectus Medialis, and m. Obliquus Dorsalis (Fig. 16e).
Function: Contraction draws the nictitating membrane posteriorly over the cornea of the eye, whereas relaxation allows the nictitating membrane to return to its resting position along the anterior edge of the eye [99, 100, 110, 114].
m. Pyramidalis Membrane Nictitans (m. PyrMemNi)
The m. Pyramidalis Membrane Nictitans is the smaller of the two muscles associated with the nictitating membrane [37, 58, 99, 100, 102]. The tendinous end is visible in the third CT dataset. We find the muscle belli to be much larger than figured by Chard and Gundlach .
Origin: The m. PyrMemNi has previously been described as arising from the ventral surface of the eye , but our segmentation suggests that the origination is anteroventral rather than strictly ventral (Fig. 16f). It is innervated by CN VI . In correspondence with previous descriptions of the pigeon , about 50% of the origin is overlapped by insertion of the m. Rectus Ventralis . This organisation contrasts with that of the sparrow (Fig. 16a; ) where the origin is entirely overlapped and in the tinamou where there is almost no overlap (Fig. 16c; ).
Path: The m. PyrMemNi has a complex course that first passes dorsally and transitions into a narrow tendon (Figs. 15a, 16f) that curves posteriorly through a sling formed by the m. QuMemNi, around CN II, and passes posteroventrally around the eye before heading anterodorsally [102, 110].
Insertion: On the posteroventral edge of the membrane nictitans (Fig. 15a).
Function: As for the m. QuMemNi, contraction draws the nictitating membrane posteriorly over the cornea of the eye, whereas relaxation allows the nictitating membrane to return to its resting position along the anterior edge of the eye [99, 110]. The involvement of both muscles, with the sling and tendon mechanism, maintains a consistent direction of pull on the pyramidalis tendon regardless of the orientation of the eye [99, 100, 110, 114].
m. Rectus Lateralis (m. RecLa)
The m. Rectus Lateralis (=external rectus of Chard and Gunlach ) lies in the posteroventral corner of the orbit and is innervated by abducens nerve (CN VI).
Origin: Like the other rectus muscles, the m. Rec La originates from a thickened periorbital tissue surrounding the optic nerve (Fig. 15c; [102, 110, 116]). The muscle origin involves two heads of equal size (Fig. 16e).
Path: It follows the medial surface of the eye (Fig. 15e).
Function: Contraction of the m. RecLa alone moves the eye posteroventrally .
m. Rectus Medialis (m. RecMe)
The m. Rectus Medialis (=internal rectus of Chard and Gunlach ) is a relatively large, flat muscle.
Origin: The anteromedial edge of a thickened periorbital tissue surrounding CN II (Fig. 15c) close to the interorbital septum. The muscle origin involves two heads (Fig. 16e). The dorsal head may be larger than that of the m. Rectus Ventralis in contrast to previous descriptions (Fig. 16d; ). It is innervated by CN III (Additional file 1).
Path: The m. RecMed is situated in the centre of the orbit close to its medial wall, dorsal to the path of CN III and superficial (lateral) to the paths of the Harderian gland and CN V1. It follows the medial surface of the eye outside the m. QuMemNi and m. PyrMemNi (Fig. 16e).
Insertion: The anterodorsal surface of the eye near the m. Obliquus Dorsalis (Fig. 16e; ). The insertion is relatively large, similar in size to that of the turkey (Fig. 16b; ) and significantly larger than that of the house sparrow (Fig. 16a; ).
Function: Contraction of the m. RecMe alone moves the eye anterodorsally .
m. Rectus Ventralis (m. RecVe)
Origin: The anteroventral edge of the thickened periorbital tissue surrounding CN II (Fig. 15c).
Path: Around the anteroventral surface of the eye overlapping the origin of the m. PyrMemNi (Fig. 16e).
Insertion: The anteroventral surface of the eye (Fig. 16e; ). The insertion is relatively similar in size to that of the house sparrow (Fig. 16a; ) and tinamou (Fig. 16c; ) but much smaller than that of the turkey .
Function: Contraction of the m. RecVe moves the eye anteroventrally .
m. Rectus Dorsalis (m. RecDo)
The m. rectus dorsalis (=superior rectus of Chard and Gunlach ) has been described as the largest of the four rectus muscles in Columba . However, as elsewhere , we find it to be smaller than the m. Rec Med (Fig. 16 e, f). On the right it was difficult to separate the m. RecDo from the m. Quadratus Membrane Nictitantis. Similarly, the m. RecDo could not be clearly identified in a digital dissection of common buzzard (Buteo buteo), suggesting that this muscle is generally difficult to distinguish .
Origin: From the posterodorsal edge of the thickened periorbital tissue surrounding CN II (Fig. 15c).
Path: It lies close the posterior wall of the orbit; it is superficial (lateral) to CN IV, but deep (medial) to CN V1 (Fig. 16e).
Function: Contraction of the m. RecDo alone causes the eye to move posterodorsally .
m. Obliquus Dorsalis (m. OblDo)
The m. Obliquus Dorsalis (=superior oblique of Chard and Gunlach  and Knox and Donaldson ) is one of two oblique muscles. On the right side it was difficult to distinguish from the m. Quadrates Membrane Nicititantis. It is the only muscle innervated by the trochlear nerve (CN IV).
Insertion: The dorsomedial edge of the eye. The posterior part of the insertion is less extensive than might be expected given previous descriptions [102, 116] but it does lie medial to that of the m. RecDo (Fig. 16e). It is notably larger than in the house sparrow (Fig. 16a; ).
Function: Rotates the eye anterodorsally.
m. Obliquus Ventralis (m. OblVe)
Path: It passes medial to the Harderian gland and m. PyrMemNi (Fig. 16e).
Function: Rotates the eye anteroventrally.
m. Levator Palpebrae Dorsalis (m. LevPalDo)
Origin: From an aponeurosis that arises from the dorsal or anterodorsal margin of the orbital boundary .
Path: It passes over the anterodorsal surface of the eye (Fig. 2a).
Insertion: Inserts on the dorsal eyelid (Fig. 2a).
Function: It opens the eyelid (Fig. 2a).
m. Levator Palpebrae Ventralis (m. LevPalVe)
Path: It passes laterally between the m. RecLat and m. PPQ and around the ventrolateral edge of the eye.
Insertion: Inserts on the anterior surface of the ventral eyelid (Fig. 2a).
Function: It opens the eyelid. It may also serve to anchor the lid and prevent it being pulled forwards with the nictitating membrane when the nictitating muscles relax .
m. Levator Palpebrae Obliquus (m. LevPalOb)
This muscle, known to occur in the tinamou (=m. orbicularis palpebrarum of ), cannot be seen in any of our CT datasets and may be absent in Columba.
The homology of diapsid neck muscles has been generally established [117, 118] and detailed descriptions of bird muscles are available . Burk  includes specific descriptions of Columba livia. Other useful descriptions of neck muscles in birds include those of the pied-billed grebe (Podilymbus podiceps) , the domestic turkey (Meleagris gallopavo) ( plates 7 to 13), and the common buzzard (Buteo buteo) .
m. Complexus (m. Cpx)
The m. Complexus of birds (e.g., [37, 108, 111]) is probably homologous with the M. Longissimus Cervicocapitis pars m. Articulo-parietalis of lepidosaurians and the m. Transversospinalis Capitis of crocodylians due to their similar points of origin and insertion . It is the most superficial neck muscle in dorsal view [58, 110].
Insertion: A crescent-shaped insertion on the back of the skull superficial to all other neck muscles along the crista nuchalis (=occipital ridge) (Fig. 8b).
Function: Mediolateral and dorsal movements of the head.
m. Biventer Cervicis (m. BivCer)
The m. biventer cervicis of birds (e.g., [37, 108, 111]) is probably homologous with the m. Spinalis Capitis of lepidosaurians and the medial part of the M. Transversospinalis Capitis of crocodylians due to their similar points of origin and insertion .
Path: Passes anteriorly and forms two distinct bellies on either side of the midline posterior to the atlas and axis (Fig. 17a).
Insertion: On the posterior surface of the parietals, deep to the m. Cpx either side of the midline (Fig. 8b).
Function: Mediolateral and dorsal movements of the head.
m. Splenius Capitis Lateralis (m. SpCapLa)
The m. Splenius Capitis of birds may be composed of two parts [58, 111, 119]. The medial part is homologous to the m. Rectus Capitis Posterior of lepidosaurians and the m. Atloïdo-capitis of crocodylians , whereas the lateral part is homologous to the m. Obliquus Capitis Magnus of lepidosaurians and the m. Epistropheo-Capitis of crocodylians . In Columba livia the two parts can be considered as separate muscles given that they have distinct sites of origin and insertion and are relatively easy to separate. An ascending branch of the CN XI passes between the ventral edges of the two parts before continuing into the body of the mSpCapL (Fig. 4b; Additional file 1).
Path: It passes anterolaterally and fans outwardly from the midline (Fig. 17c, d).
Function: Mediolateral and dorsal movements of the head.
m. Splenius Capitis Medialis (m. SpCapMe)
Path: It passes anterolaterally and fans outwardly from the midline (Fig. 17c, d).
Insertion: It inserts ventromedial to the m. SpCapL and lateral to the m. BivCer and foramen magnum (Fig. 8b).
Function: Mediolateral and dorsal movements of the head.
m. Rectus Capitis Lateralis (m. ReCapLa)
The m. Rectus Capitis Lateralis of birds (e.g., [37, 108, 110]) is homologous to the dorsal part of the m. Rectus Capitis Anterior in lepidosaurians and the m. Iliocostalis Capitis of crocodylians . It is broad and conspicuous in lateral view and appears to be innervated by CN XII.
Path: It passes dorsolaterally overlapping the m. Cpx close to its insertion but not as much as in Buteo buteo .
Insertion: The posterolateral edge of the cranium between the insertion for the m. SpCapLat and the m. DM (Fig. 14). It has a long slightly sigmoid insertion.
Function: Mediolateral movements of the head.
m. Rectus Capitis Ventralis (m. ReCapVe)
The m. rectus capitis ventralis is homologous to the ventral part of m. Rectus Capitis Anterior in lepidosaurians and the m. Rectus Capitis Anticus Major of crocodylians .
Origin: The medial part originates from the ventral surface of the atlas, axis, as well as more posteriorly located vertebrae . The origin of the lateral part is not present in our specimen but in other taxa derives from the third, fourth, and possibly fifth vertebrae .
Insertion: On the ventral surface of the basioccipital (Fig. 8b).
Function: Ventral movements of the head.
m. Rectus Capitis Dorsalis (m. ReCapDo)
The m. Rectus Capitis Dorsalis is one of the deepest hypaxial muscles .
Origin: The dorsal part originates from the posterolateral surface of the atlas, axis (Figs. 17d, 18b) as well as vertebrate located more posteriorly along the neck , often as far back as the 5th vertebra .
Path: It passes rostrally lateral to the atlas and axis.
Insertion: Three heads insert on the ventral surface of the cranium (Fig. 18b), posterior to the m. RecCapVe but medial to the exit of CN X and anterior to the exits of CN XII (; Additional file 1). The three heads are also visible in Eudromia elegans, the elegant crested tinamou (: Fig. 14).
Function: Ventral movement of the head.
m. Flexor Colli (m. FlexCol)
This deep epaxial muscle is relatively small .
Path: It passes rostrally close to the midline ventral to the neck vertebrae (Fig. 18c).
Insertion: On the posteroventral surface of the atlas and possibly also the anterolateral surface of the axis (Fig. 18c).
Function: Contraction of this muscle would move the front of the neck posteroventrally.
m. Interspinales (m. Interspin)
There is clearly muscle spanning the dorsal halves of the atlas and axis, and this is likely part of the Interspinales . There appears to be medial and lateral portions that are contiguous with one another (Additional file 1).
Origin: The medial portion originates from the lateral surface of the neural spine of the axis whereas the lateral part originates from the dorsal surface of the neural arch of the axis (Fig. 17d).
Path: The medial potion passes anterolaterally whereas the lateral portion passes anteroventrally.
Insertion: The medial portion inserts on the posterior surface of the posterolateral edge of the atlas whereas the lateral portion inserts on the posterolateral prominence of the atlas (Fig. 17d).
Function: Supporting connection between the axis and atlas.
In this paper, we present a 3D digital dissection of the head of Columba livia, the rock dove, one of the most numerous, widespread and morphologically disparate avian species in the world, and use these data to describe its cranial and anterior cervical musculature. This was accomplished by applying the emerging technique of diceCT, combining contrast-enhancement of soft tissues using staining agents, CT scanning, and powerful visualization software. DiceCT has number of advantages over other methods, as it is non-destructive, replicable, and suitable for small and fragile specimens. It preserves the 3D topological relationships between anatomical structures and provides a powerful means of visualisation and communication that can provide an important tool to complement classical dissections (e.g., [30, 32, 33, 97, 120]). This approach is particularly good at providing the shape of the muscle and facilitating accurate communication regarding their relative positions to one another. It is also arguably easier for the anatomical work to be shared among a larger team of people . However, there are also limitations such as the absence of colour, the difficulty interpreting aponeuroses, and occasionally problems inferring the precise origin/insertion of a muscle when it passes closely over a bony surface. Nevertheless, it is objectively more informative than a limited number of coronal and horizontal sections where the boundaries between individual muscles are not indicated (e.g., ).
Our interpretations and divisions of the jaw muscles most closely resemble those of van Gennip , in particular those relating to the structure of m. Adductor Mandibular Externus and m. Pterygoid Dorsalis. In contrast to previous studies (e.g., [30, 33]), we did not find a clear division of the m. Depressor Mandibulae and m. Pterygoideus Ventralis. However, we identify a division within the m. Adductor Mandibulae Externus pars Medialis not previously described. We were also able to successfully separate the m. Adductor Mandibulae Posterior from the m. Adductor Mandibulae Externus pars Medialis despite problems previously encountered . As previous interpretations have suggested  the jaw muscles of Columba livia are less extensive that those of some other columbiform taxa [25, 30, 40] and this might reflect feeding behaviour related to dietary differences. Our digital dissection of the throat muscles corresponds to those of Bhattacharyya  and Zweers  and is consistent with the homologies inferred for chicken based on developmental observations . Our interpretation of pigeon eye muscles clarifies the description of Chard and Gunlach  and highlights significant differences that exist between the eye muscles among avian taxa. We show that that muscle arrangement and relative size in C. livia are more similar to that of the turkey ), and particularly the tinamou  (Table 4), rather than that of the house sparrow . How much these differences reflect phylogenetic inheritance, size, and lifestyle requires wider comparisons.
Columba livia is an important model organism across biological sciences and we will use these anatomical data for biomechanical analyses of the pigeon feeding system. This muscle arrangement can be simplified into a finite number of strands that enable explicit reporting of origins and insertions [47, 50]. It can also be used for multibody dynamics analysis to quantitatively test specific hypotheses regarding jaw movement and possibly gape [48, 51–53, 123] and coupled with Finite Element Analysis to examine the distribution of strain and structural deformation during feeding (e.g., [45, 59, 84, 124]). These approaches are highly amenable to sensitivity analyses and therefore extremely powerful for understanding the effects of parameters within models and the context of results. Moreover, the phylogenetic position of C. livia means that this study provides crucial data for reconstructing cranial tissues in extinct archosaurs [80, 81, 83], facilitating biomechanical analyses of morphological trends observed in the fossil record (e.g., ) or of novel skull structures lying outside the range of extant phenotypic diversity. (e.g., ).
Our digital dissection of C. livia (and those of Buteo buteo  and Dacelo novaeguineae ) provides a starting point for a wider digital survey of avian cranial muscle anatomy to compliment previous work e.g., [30, 33] and investigate patterns of evolution. The hyoid apparatus and eye muscles alone have great potential for valuable phylogenetic characters and as well as indicators of life habit that can be compared across clades (with independent contrasts). Now that the systematic relationships of birds are becoming increasing well understood [87, 88], and analytical tools are increasingly more powerful (e.g., [125–129]), there is great opportunity for a richer understanding of how phenotype might have underpinned their diversity and success.
Our 3D model is fully available, making it of use to other researchers, in anatomical, morphometric or taxonomic studies, as well as in education and outreach. Digital dissection is more palatable and accessible to the public than gross dissection, and provides an excellent starting point for students investigating comparative anatomy. The surface files from our digital dissection could be enlarged and printed in three dimensions to provide a further resource for research, communication, and teaching (e.g., [92, 130, 131]). The durable nature of such models means that they can be used repeatedly, and their colourful nature makes them attractive teaching or outreach tools, and a stepping stone to handling actual specimens. The kinaesthetic nature of the models has the potential to provide a more effective learning experience, particularly for those with sensory disabilities, especially given research suggesting that multi-sensory input (here = visual + tactile) improves memory performance .
The pigeon material was donated by John R. Hutchinson and Jim Usherwood (Royal Veterinary College, Hatfield, UK). Advice on staining was provided by Jen Bright (University of South Florida, USA), Philip Cox (University of York, UK), Paul Gignac (Oklahoma State University, USA) and Stephan Lautenschlager (University of Birmingham, UK). Access to CT-scanning facilities was provided by Robert Asher and Colin Shaw (University of Cambridge, UK) and Tom Davies (University of Bristol, UK). For valuable assistance with obtaining literature, we thank staff at the Natural History Museum, UK. Technical support for Avizo was provided by Alejandra Sánchez-Eróstegui (Thermo Fisher Scientific), Alex Ball, Vincent Fernandez, and Brett Clark (all Core Research Laboratories, Natural History Museum London, UK). Feedback from two anonymous reviewers and Casey Holliday (Universtiy of Missouri, USA) improved this manuscript. The authors have no competing interests to declare.
This research was supported by a NERC grant NE/R000077/1 (‘The role of cranial biomechanics and feeding in clade diversification and early dinosaur evolution’) awarded to PMB and LBP.
Availability of data and materials
The primary datasets for this article are the 3D PDFs, which have been uploaded as part of the supplementary material (Additional file 1). Reconstruction in other 3D formats are available upon request to the corresponding author.
MEHJ, PMB, and LBP designed the study; LBP carried out specimen staining and CT-scanning; MEHJ segmented and interpreted the CT data, created 3D PDFs and drafted the original manuscript. All authors contributed to revisions of the manuscript and gave final approval for publication.
Ethics approval and consent to participate
The specimen of Columba livia was sourced from Jim Usherwood and John Hutchinson (Royal Veterinary College, Hatfield, UK) having formed part of an unrelated study. It was not collected solely for the purpose of this research and, consequently, observance of animal care protocols was not required for this study.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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