(13)  Musculi bulbi oculi.  There are six extrinsic muscles of the avian eyeball, arranged as three opposing pairs:  Mm. rectus dorsalis and rectus ventralis; Mm. rectus lateralis and medialis; Mm. obliquus dorsalis and obliquus ventralis; see Fig. 6.2.  All six muscles attach on the cranium (Septum interorbitale) and insert on the Sclera. They are innervated like their mammalian counterparts (PNS Fig. 2; Bubien-Waluszewska,1981) and function in direct movements (positioning) of the eyeball. Although there is no trochlea associated with the distal end of  M. obliquus dorsalis, this muscle is in all probability a homologue of M. obliquus superior of the mammalian eye.

    For a comprehensive review of these muscles in several avian taxa, see Abraham and Stammer (1966), Zusi and Bentz (1984), and Elzanowski (1987).   McVean et al. (1987) describe the muscle fiber types which are present in these muscles in Columba.

 

(14) Musculi membranae nictitantis.  There are two muscles characterized by having attachments (origin) on the sclera of the eyeball (Fig. 6.02B), and insertions in the nictitating membrane. The aponeurosis of M. quadratus membranae nictitantis is reflected on itself to form a fibrous sheath (Vagina tendinis) which facilitates passage of the tendon of  M. pyramidalis membranae nictitantis as the latter arches over N. opticus (Slonaker,1918; Simic and Jablan-Pantic,1959; Elzanowski,1987).  The innervation of these muscles from N. abducens is well reviewed and illustrated by Bubien-Waluszewska (1981); see Sens. Annot. ___ ;   PNS Annot. 16; PNS Fig. ___, and Martin (1985).

 

(15) Musculi palpebrarum et periorbitae. In addition to the six extrinsic muscles of the eyeball (Annot. 14) which attach on the interorbital septum, a striated muscle for the upper eyelid (M. levator palpebrae dorsalis) and lower eyelid  (M. depressor palpebrae ventralis), and a muscle of the floor of the orbit  (M. tensor

periorbitae), also originate on the interorbital septum.  M. levator palpebrae dorsalis inserts in the marginal folds (Plicae marginales dorsales, Sens. Annot. ___) of the upper eyelid; it is innervated by the dorsal ramus of the oculomotor nerve (PNS Fig. ___; Bubien-Waluszewska,1981).  M. depressor palpebrae ventralis inserts on the proximal edge of the fibrous tarsus of the lower eyelid.  M. tensor periorbitae forms a muscular floor of the orbit in the form of a muscular sling separating the orbital contents from the jaw muscles (Elzanowski,1987).   The latter two muscles are innervated by a branch from the mandibular nerve (PNS Annot. ___ ; Bubien-Waluszewska,1981).

    Nonstriated muscle fibers which are arranged approximately parallel to the free margins of the eyelids form  M. orbicularis palpebrarum (Sens., Palpebrae).

 

(16) Only a single muscle, M. columellae, has been described in the avian middle ear; for additional information, see Sens., Fig. 16.3 and Annot. 52, and Elzanowski, 1987.

 

(17)  Musculi mandibulae.  A collective term for those muscles which are involved in opening and closing the jaws (Fig. 6.4); individual muscles are named after Lakjer (1926).  They have been described in several ways:  (1) on the basis of the arrangement of their fasciculi to their constituent aponeuroses (after Gans and Bock, 1965); (2) on the basis of their position relative to the facial and craniofacial articulations (Bock, 1968), and (3) on the basis of their causal role in kinetics of the avian skull (Bock, 1964; Zweers, 1974).  See Fig. 6.5  for an illustration of attachments on the skull.  With the exception of M. depressor mandibulae (Annot. 24), they are derived from the muscle primordium associated with the mandibular arch (McClearn and Noden,1988) and are innervated by N. mandibularis (PNS. Annot. 13).

 

(18)  M. adductor mandibulae externus.  Synonymy:  M. masseter superficialis, medius and profundus (Fujioka,1963).  This muscle complex consists of several aponeuroses of attachment to the cranium, and another series of aponeuroses attached to the mandible (Zweers,1974; van Gennip,1986).  Three main subdivisions are described, one or more of which may also be subdivided, but the muscle functions to close the lower jaw (Buhler,1981); see Fig. 6.05.

Pars rostralis [temporalis] (=superficialis, Lakjer,1926; superficialis or lateralis, Dzerzhinsky and Yudin,1982) is often subdivided for descriptive purposes into a temporal and an orbital subdivision.  The temporal subdivision is the more extensive and attaches on Proc. zygomaticus and extensively caudal and dorsal to it (see Fossa temporalis, Osteo. Annot. 102, 104; Mem. temporalis, Arthr. Annot. 31).  In some taxa (e.g.,  Phalacrocorax, Anhinga),  this subdivision is significantly hypertrophied and includes a prominent occipital attachment (Crista nuchalis transversa, Osteo. Annot. 17) with a separately derived head, Caput nuchale, attaching on the dorsal midline of the cranial cervical region by way of a fibrous septum in which is embedded an accessory ossification, Os nuchale (Osteo. Annot. 76;  Dullemeijer,1951; Owre,1967).  The orbital subdivision extends rostrad to attach on the caudal wall of the orbit (see  Osteo. Annot. 29; van Gennip,1986).  Pars rostralis inserts on Proc. coronoideus (Osteo. Annot. 44) of the mandible .

Pars ventralis [medialis, Lakjer,1926] is the "central" and, in some cases, the largest division, with multiple fleshy slips.  A complex aponeurosis of origin attaches on Proc. postorbitalis (Osteo., Annot. 30) including Lig. postorbitale, and Proc. zygomaticus (Osteo. Annot. 102).   Pars ventralis inserts on a clearly defined area on the caudolateral face of the mandible (see van Gennip,1986).

            Pars profunda [caudalis] (Lakjer,1926; "profundus", including "caudalis," Dzerzhinsky and Yudin,1982) is typically the smallest division and may be variable in development (e.g., Zusi and Bentz,1984).  When present as a separate division (McClearn and Noden, 1988), it attaches on the body and otic process of the quadrate, lateral to and sometimes almost inseparable from attachments of M. adductor mandibulae ossis quadrati except for a fibrous gap through which passes a motor branch of the mandibular nerve (R. pterygoideus, PNS Annot. 13; Lakjer,1926; Barnikol,1953).  The insertion of Pars profunda on the mandible, between Fossa articularis quadrati and Proc. coronoideus (Osteo. Annot. 44), is, however, independent from the insertion of M. adductor mandibulae ossis quadrati (Annot. 20).

 

(19)  M. pseudotemporalis superficialis.  Synonymy:  M. temporalis (Fujioka, 1963; Watanabe and Yasuda,1970).  M. pseudotemporalis superficialis has been considered the most lateral (at its origin) of the so-called "adductor mandibulae internus" subsystem of muscles (including Mm. pseudotemporalis profundus, adductor mandibulae ossis quadrati, pterygoideus and ethmomandibularis, Annot. 20, 21, and 22, but see also Elzanowski,1987).  In some taxa, M. pseudotemporalis superficialis attaches primarily on Area muscularis aspera (Osteo. Annot. 89) of Os laterosphenoidale, the attachment which seems to be the oldest phylogenetically, according to Hofer (1950).  It is separated from M. adductor mandibulae externus, pars rostralis, by N. maxillaris and the Rete mirabile ophthalmicum (Dzerzhinsky and Yudin,1982) and, in part, also by R. pterygoideus (PNS Annot. 13) of N. mandibularis (van Gennip,1986).  The muscle inserts on Tuberculum pseudotemporale (Osteo. Annot. 45).  See Fig. 6.5.

 

(20)  M. pseudotemporalis profundus.  Synonymy:  M. quadratomandibularis (Fujioka,1963; Hofer, 1950; Elzanowski, 1987).  M. adductor mandibulae ossis quadrati.  Synonymy:  M. adductor mandibulae "posterior" of many authors; not to be confused with pars profunda of M. adductor mandibulae externus (Annot. 18).  Both muscles form a "quadrate" portion of an "adductor mandibulae internus" muscle subsystem. 

            The relative development of M. pseudotemporalis profundus is proportional to that of Proc. orbitalis quadrati on which it has a primary (functional?) attachment (Hofer,1950).  The attachment on the quadrate is rostral to that of M. adductor mandibulae ossis quadrati from which it is separated by a fibrous gap through which passes the pterygoid ramus of the mandibular nerve (R. pterygoideus, PNS Annot. 13; Lakjer, 1926; Barnikol, 1953).  The attachment on the mandible is rostral to Proc. coronoideus and to the attachments of the other jaw muscles (in Columba, van Gennip,1986).  For additional observations in other taxa see Burton (1974c) and Bhattacharyya (1989).

            M. adductor mandibulae ossis quadrati has a primary attachment on the body of the quadrate, rostral and deep to the attachments of M. adductor mandibulae externus, pars profunda (see Annot. 18).  The attachment on the mandible lies between Tuberc. pseudotemporale (Osteo. Annot. 45), laterally, and M. pterygoideus, medially (see Annot. 21), and is separate from both of these muscles as well as from all other jaw muscles (Elzanowski,1987).

            M. pseudotemporalis profundus should be considered functionally independent from M. adductor mandibulae ossis quadrati (see Fig. 6.5, and Annot. 21; Bock,1964; Buhler,1981).

 

(21)  M. pterygoideus.  Synonymy:  M. adductor mandibulae internus (Hofer,1950).  M. pterygoideus is the "palatopterygoid" portion of an "adductor mandibulae internus" subsystem, i.e., defined by the attachments are on the palatine and pterygoid bones (Figs. 6.5).  Various subdivisions have been described:  (1) pars dorsalis and pars ventralis, each of which has lateral and medial subdivisions (Lakjer,1926); (2) three principal aponeuroses and pars lateralis, pars centralis medialis, pars dorsalis medialis ( Zusi,1962; Burton,1974a,c), or (3) pars centralis, pars dorsalis lateralis, pars dorsalis medialis, and pars retractor, the latter a separate slip which attaches on the braincase (Lamina parasphenoidalis, Richards and Bock,1973).  Pars dorsalis medialis (Zusi and Bentz,1984), which is also described as pars dorsalis rostralis (van Gennip,1986), is the only portion which seems to be more or less well-defined in many taxa (see also Elzanowski, 1987).  The muscle inserts primarily on the caudomedial aspect of the mandible and Proc. medialis mandibulae, however, the insertion may also extend to the ventrolateral aspect of the mandible ("venter externus", described by Burton,1974c and Bhattacharyya,1989; see also van Gennip, 1986). 

    M. pterygoideus and M. pseudotemporalis profundus (Annot. 20) simultaneously close both the upper and lower jaws, functioning over the force lever arm of the quadrate/pterygoid/palatine/ jugal bar axis, in addition to other functions (Buhler,1981).

 

(22)  M. ethmomandibularis. Derived from M. pterygoideus and characteristic of the Psittaciformes, it has an extensive attachment on the interorbital septum and on the medial face of the mandible.  It is important in generating biting forces during elevation of the lower jaw, as well as chewing forces by forward translation of the lower jaw, distinctive characteristics of the  feeding system of psittacines (Hofer, 1950; Burton,1974c; Homberger,1980,1986).

 

(23)  M. protractor pterygoidei et quadrati.  Synonymy;  M. craniopterygoquadratus (Fujioka, 1963); M. sphenopterygoquadratus (Dubale, 1969; Rawal, 1971).  Although Lakjer (1926) described two muscles, M. protractor pterygoidei sensu stricto  and M. protractor quadrati, both attaching on the base of the interorbital septum, these are best considered as one muscle having two parts, defined primarily on the their respective insertions, namely on Os pterygoideum and Quadratum, respectively (Fig. 6.4,5; see Figs. 13 and 16 in Bhattacharyya, 1982, for illustration of the attachments).  The muscle forces are exerted on the "palatoquadrate bridge" to protract and open the upper jaw (Buhler,1981; see Bock,1966 for the specific configuration in woodpeckers).

 

(24)  M. depressor mandibulae.  Synonymy:  M. occipitomandibularis (Fujioka, 1963); M. digastricus (Berger,1966).  The cranial attachment largely fills the Fossa subtemporalis (Osteo. Annot. XXX) between Crista nuchalis transversa and Fossa temporalis on the squamous portion of the calvaria (Fig. 6.4,5,6).  It extends ventrally over the lateral surface of Proc. paroccipitalis. Medially the muscle also has an extensive attachment on Membr. postmeatica and ventromedially on Lig. occipitomandibulare (Arthr. Annot. 37).  The muscle inserts in Fossa caudalis of the mandible (Osteo. Annot. 51)., including also Fossa conicalis and Proc. retroarticularis when these bony structures are present (e.g., Anas, Zweers,1974) .   The muscle is innervated by a specific branch from N. hyomandibularis of the facial nerve (PNS Annot. 23), and may consist of more than one part, each distinct and separable, with different functional roles (Bock,1964; Zusi,1967; Zweers,1974).  Buhler (1970, and pers. comm.) suggests that, in the Caprimulgidae, an internal head, which is fused with Lig. occipitomandibulare (Arthr. Annot. 37 ; Osteo. Annot. 51), may not be part of this muscle set.