A Study of the Head during Prenatal and Perinatal Development of Two Fetuses and One Newborn Striped Dolphin (Stenella coeruleoalba, Meyen 1833) Using Dissections, Sectional Anatomy, CT, and MRI: Anatomical and Functional Implications in Cetaceans and Terrestrial Mammals

Abstract

Our objective was to analyze the main anatomical structures of the dolphin head during its developmental stages. Most dolphin studies use only one fetal specimen due to the difficulty in obtaining these materials. Magnetic resonance imaging (MRI) and computed tomography (CT) of two fetuses (younger and older) and a perinatal specimen cadaver of striped dolphins were scanned. Only the older fetus was frozen and then was transversely cross-sectioned. In addition, gross dissections of the head were made on a perinatal and an adult specimen. In the oral cavity, only the mandible and maxilla teeth have started to erupt, while the most rostral teeth have not yet erupted. No salivary glands and masseter muscle were observed. The melon was well identified in CT/MRI images at early stages of development. CT and MRI images allowed observation of the maxillary sinus. The orbit and eyeball were analyzed and the absence of infraorbital rim together with the temporal process of the zygomatic bone holding periorbit were described. An enlarged auditory tube was identified using anatomical sections, CT, and MRI. We also compare the dolphin head anatomy with some mammals, trying to underline the anatomical and physiological changes and explain them from an ontogenic point of view.

Keywords: MRI; PET/SPECT/CT; fetal development; head anatomy; ontogenesis; sectional anatomy; striped dolphin (Stenella coeruleoalba).

Figure 1

Approximated level sections of fetus dolphin head. Lines represent the location for each transverse anatomical section, CT, and MR images (I–VII).

Figure 2

Representative transverse images of the snout made at the level of the rostral portion of the melon and oral cavity. Level I. Images are oriented so that the left side of the head is to the right and dorsal is at the top. Row (from now on R) 1, sco1; R2, sco2; R3, sco3. (A) Anatomical section. (B) Vascular window PET/SPECT/CT image. (C) Soft-tissue window CT image. (D) T1-weighted SE sequence. (E) T2-weighted fast spin echo (FSE) sequence. (F) T1-weighted fast field echo (FFE) sequence. (G) T1-weighted out of phase (OOP) gradient echo (GRE) sequence. 1, Mesethmoid cartilage; 2, incisive bone; 3, maxillary bone; 4, vomer bone; 5, supraorbital canal; 6, mandible; 7, canal and mandibular fat; 8, tooth in development; 9, socket of tooth; 10, oral cavity; 11, oral vestibule; 12, tongue; 13, melon; 14, melon rostral muscles; 15, mylohyoid muscle; 16, buccinator and depressor of the lower lip muscles; 17, lateral sublingual recess; 18, epidermis and dermis.

Figure 3

Representative transverse images made at the level of root of the snout, caudal portion of the melon, and oral cavity. Level II. Images are oriented so that the left side of the head is to the right and dorsal is at the top. R1, sco1; R2, sco2; R3, sco3. (A) Anatomical section. (B) Vascular window PET/SPECT/CT image. (C) Soft-tissue window CT image. (D) T1-weighted SE sequence. (E) T2-weighted FSE sequence. (F) T1-weighted FFE sequence. (G) T1-weighted OOP GRE sequence. 1, Mesethmoid cartilage; 2, incisive bone; 3, maxillary bone; 4, vomer bone; 5, frontal bone; 6, lacrimal bone; 7, zygomatic bone; 8, lacrimal-zygomatic synchondrosis; 9, zygomatic bone: temporal process; 10, maxillary sinus; 11, palatine bone; 12, mandible; 13, canal and mandibular fat; 14, melon; 15, tongue; 16, oral cavity; 17, melon rostral muscles; 18, pterygoid muscles; 19, mylohyoid muscle; 20, digastric muscle; 21, fat and striated muscle; 22, epidermis, dermis and subcutaneous tissue; 23, nostrils.

Figure 4

Representative transverse images made at the level of nasal, oral cavities, and orbital craniofacial fossa. Level III. Images are oriented so that the left side of the head is to the right and dorsal is at the top. R1, sco1; R2, sco2; R3, sco3. (A) Anatomical section. (B) Vascular window PET/SPECT/CT image. (C) Soft-tissue window CT image. (D) T1-weighted SE sequence. (E) T2-weighted FSE sequence. (F) T1-weighted FFE sequence. (G) T1-weighted OOP GRE sequence. 1, Mesethmoid cartilage; 2, incisive bone; 3, maxillary bone; 4, vomer bone; 5, lacrimal bone; 6, zygomatic bone: temporal process; 7, palatine bone; 8, pterygoid bone; 9, ethmoid bone; 10, mandible; 11, canal and mandibular fat; 12, periorbit and eyeball; 13, tongue; 14, melon external fiber ring; 15, digastric muscle; 16, pterygoid muscle; 17, mylohyoid muscle; 18, oral cavity; 19, melon caudal muscles; 20, frontal bone: orbital recess; 21, pterygopalatine recess; 22, fat and striated muscle; 23, nostrils; 24, nasal diverticulum and nasal plug (arrow); 25, membranous part of nasal septum; 26, nasal cavity; 27, nasal mucosa; 28, melon; 29, nasal vestibule muscles.

Figure 5

Representative transverse images made at the level of the rostral part of the cranial cavity, choanas, and eyeball. Level IV. Images are oriented so that the left side of the head is to the right and dorsal is at the top. R1, sco1; R2, sco2; R3, sco3; (A) Anatomical section. (B) Vascular window PET/SPECT/CT image. (C) Soft-tissue window CT image. (D) T1-weighted SE sequence. (E) T2-weighted FSE sequence. (F) T1-weighted FFE sequence. (G) T1-weighted OOP GRE sequence. 1, Incisive bone; 2, maxillary bone; 3, frontal bone; 4, vomer bone; 5, presphenoid bone: body and wings; 6, palatine bone; 7, pterygoid bone; 8, basisphenoid bone: pterygoid crest; 9, zygomatic bone: temporal process; 10, ethmoid bone; 11, mandible; 12, eyeball; 13, sclera; 14, lens; 15, eyelids; 16, lateral pterygoid muscle; 17, medial pterygoid muscle; 18, choanae and nasopharyngeal sphincter muscle; 19, tongue; 20, oral cavity; 21, pterygopalatine recess; 22, digastric muscle; 23, subarachnoid space; 24, longitudinal brain fissure; 25, brain: frontal lobe; 26, mandibular canal; 27, mylohyoid muscle; 28, hyoglossus muscle; 29, extraocular muscles; 30, melon caudal muscles; 31, frontal bone: orbital recess; 32, nasal diverticulum; 33, fat and striated muscle.

Figure 6

Representative transverse images made at the level of the pharynx and the caudal part of the orbit. Level V. Images are oriented so that the left side of the head is to the right and dorsal is at the top. R1, sco1; R2, sco2; R3, sco3. (A) Anatomical section. (B) Vascular window PET/SPECT/CT image. (C) Soft-tissue window CT image. (D) T1-weighted SE sequence. (E) T2-weighted FSE sequence. (F) T1-weighted FFE sequence. (G) T1-weighted OOP GRE sequence. 1, Nasal bone; 2, maxillary bone; 3, frontal bone; 4, vomer bone; 5, presphenoid bone: body; 6, presphenoid bone: wings; 7, palatine bone; 8, pterygoid bone: hook-like process; 9, pterygoid bone: pterygoid crest; 10, mandible; 11, eyeball; 12, lens; 13, optic nerve; 14, sclera; 15, cornea; 16, eyelids; 17, lateral pterygoid muscle; 18, medial pterygoid muscle; 19, nasopharynx and nasopharyngeal sphincter muscle; 20, pterygopalatine fossa; 21, subarachnoid space; 22, longitudinal brain fissure; 23, brain: temporal lobe; 24, mandibular canal; 25, digastric muscle; 26, sternohyoid muscle; 27, fat and striated muscle; 28, melon caudal muscles; 29, extraocular muscles; 30, temporomandibular joint; 31, auditory tube; 32, pharyngeal opening of the auditory tube; 33, oropharynx; 34, tongue; 35, frontal bone: orbital recess; 36, zygomatic bone: temporal process; 37, brain: lateral ventricle; 38, sagittal dorsal sinus; 39, epidermis, dermis, and subcutaneous tissue.

Figure 7

(A) Superficial and (B) middle head dissection made after removing melon and fat of sco5. 1, Melon; 2, mylohyoid muscle; 3, buccinator and depressor of the lower lip muscles; 4, fat and striated muscle; 5, digastric muscle; 6, geniohyoid muscle; 7, sternohyoid and sternothyroid muscles; 8, orbicularis oculi muscle; 9, external acoustic meatus (cartilaginous); 10, mandible: body; 11, subcutaneous tissue; 12, maxillary vein.

Figure 8

Representative transverse images at the level of the cranial vault of the skull involving the temporal lobe of the brain, mesencephalon, middle and inner ear, larynx and hyoid apparatus. Level VI. Images are oriented so that the left side of the head is to the right and dorsal is at the top. R1, sco1; R2, sco2; R3, sco3. (A) Anatomical section. (B) Vascular window PET/SPECT/CT image. (C) Soft-tissue window CT image. (D) T1-weighted SE sequence. (E) T2-weighted FSE sequence. (F) T1-weighted FFE sequence. (G) T1-weighted OOP GRE sequence. 1, Occipital bone: basilar part; 2, pterygoid crest; 3, temporal bone: tympanic part; 4, temporal bone: petrous part; 5, auditory ossicles of middle ear (malleus and incus); 6, auditory ossicles of middle ear (stapes); 7, auditory ossicles of middle ear (incus); 8, frontal process of temporal bone; 9, squamous part of temporal bone; 10, parietal bone; 11, interparietal bone; 12, tympanohyoid cartilage; 13, stylohyoid bone; 14, thyrohyoid bone; 15, basihyoid bone; 16, middle ear: tympanic cavity; 17, middle ear: musculotubarius canal; 18, inner ear: cochlea (spiral canal); 19, inner ear: vestibule; 20, arytenoid cartilage; 21, epyglotic cartilage; 22, nasopharynx: intrapharyngeal orifice; 23, laryngopharynx: piriform recess; 24, ramus of the mandible: condylar process; 25, temporal muscle; 26, mesencephalon: tegmentum; 27, mesencephalon: aqueduct; 28, mesencephalon: colliculus; 29, lateral ventricles; 30, corpus callosum; 31, falx cerebri; 32, dorsal sagittal sinus; 33, sinus transversus; 34, brain hemisphere: temporal lobe; 35, cerebellum: cerebellar hemispheres; 36, meninx: cerebellar tentorium; 37, facial and vestibulocochlear nerves and labyrinthic artery; 38, orifice and internal acoustic meatus; 39, sternohyoid muscle; 40, external acoustic meatus: cartilaginous rudiment; 41, peribullar sinus; 42, fontanelles; 43, epidermis, dermis, and subcutaneous tissue.

Figure 9

Deep head dissection made at the level of the nasal vestibule and melon of sco4. 1, Melon: nucleus; 2, melon: external fiber ring; 3, melon rostral muscles; 4, melon caudal muscles; 5, right nasal cavity (after removing nasal plug); 6, left nasal plug; 7, maxillary bone; 8, ethmoid bone; 9, nasal septum.

Figure 10

Representative transverse images made at the level of the occipital bone, cerebellum, and trunk of encephalon. Level VII. Images are oriented so that the left side of the head is to the right and dorsal is at the top. R1, sco1; R2, sco2; R3, sco3. (A) Anatomical section. (B) Vascular window PET/SPECT/CT image. (C) Soft-tissue window CT image. (D) T1-weighted SE sequence. (E) T2-weighted FSE sequence. (F) T1-weighted FFE sequence. (G) T1-weighted OOP GRE sequence. 1, Occipital bone: lateral part; 2, occipital bone: squamous part; 3, occipital bone: basilar part; 4, myelencephalon; 5, cerebellum: vermis; 6, cerebellum: cerebellar hemispheres; 7, subarachnoid space; 8 = esophagus; 9, laryngeal cavity: glottis; 10, vascular and nerve structures of the pharynx and larynx; 11, external jugular vein; 12, longus capitis muscle; 13, scapula; 14, sternohyoid and sternothyroid muscles; 15, cleidocephalic muscle: mastoid part; 16, sternocephalic muscle: mastoid part; 17, longissimus capitis muscle; 18, splenius capitis muscle; 19, semispinalis capitis muscle (digastric); 20, semispinalis capitis muscle (complex); 21, spinalis capitis muscle; 22, epidermis, dermis, and subcutaneous tissue; 23, fontanelles.