This description focuses primarily on UALVP 47977, as it best presents new information. This paper largely follows Witmer (1995, 1997), Evans (2006) and Witmer & Ridgely (2008) for homologies in the antorbital region (Figs 1 and 2). The nasal cavity refers to a respiratory and olfactory passage that extends between the external naris and the choana, and is equivalent to the respiratory tract, the respiratory passage and the airway in other papers.
Figure 2. Illustration (A) and photograph (B) of the ventral view of an ankylosaurid skull roof (UALVP 47977, Euoplocephalus) from the Dinosaur Park Formation (Campanian, Upper Cretaceous), southern Alberta. Hatched lines indicate parts reconstructed with plaster. Impressions of the soft tissues, including the main airway, nasal arteries, and possible turbinates, are well defined. The ethmoidal elements are well ossified and separate regions of the nasal cavity from each other. No sutures are visible. aw, anterior wall of the cavity for the olfactory region; cor, cavity for the olfactory region; ls, laterosphenoid; od, orbital depression; sl, sulcus associated with the groove in the olfactory region. For other abbreviations, see Fig. 1.
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In UALVP 47977, the dorsal surface of the skull is moderately weathered. The specimen preserves the top and lateral parts of the nasal cavity, which represent both the non-olfactory and olfactory regions of the nasal cavity (Fig. 2; Witmer & Ridgely, 2008). As in most ankylosaurs, but unlike Cedarpelta (Carpenter et al. 2001) and Pinacosaurus (Maryańska, 1977), no sutures can be observed. The non-olfactory dorsomedial passage of the nasal cavity under the frontals extends posteriorly behind the orbits, just anterior to the braincase. The olfactory region of the nasal cavity occupies the large cavity on both sides of the non-olfactory dorsomedial passage. A well developed bony wall separates the dorsomedial passage from the olfactory region for all its preserved length.
The dorsomedial passage of the nasal cavity (main airway) is divided into right and left passages by the nasal septum. There is no evidence for a median common chamber as reconstructed for lambeosaurine ornithopods (Evans et al. 2009). On both the lateral and medial walls of the nasal cavity proper in UALVP 47977, deep grooves extend anteroposteriorly and lead to the extensive vascular impressions in the roof of the nasal cavity (Fig. 3). The impressions branch and extend posteromedially toward the nasal septum and this pattern is bilaterally consistent. The vascular impressions are conspicuous in the anterior half of the preserved length of the main airway but are absent in the posterior half. Vascular impressions are also preserved in this region in AMNH 5238. Vascular impressions could not be reconstructed from the CT scans of AMNH 5405 and UALVP 31, but this is because of inadequate resolution of the CT scans.
Figure 3. Vascular impressions in the dorsomedial part of the nasal cavity proper of UALVP 47977. (A) Drawing of skull showing region of enlargement in diagram (B) and photograph (C). These ethmoidal vessels are likely to be part of the median nasal canal system. Hatched area in B represents broken nasal septum (mesethmoid). Anterior is to the right. For abbreviations, see Fig. 1.
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The cavity that housed the olfactory region of the nasal cavity occupies a large volume to the side of the dorsomedial part of the main airway. The cavity is surrounded by a thin sheet of bone (ectethmoid) laterally and by thick bony walls medially and anteriorly, and is connected posteriorly with the endocranial cavity through the olfactory fenestra. The olfactory bulb sat within this fenestra through which the olfactory nerves [cranial nerve (CN) I], ethmoidal vessels and their branches passed. This fenestra was previously identified as an olfactory tract in Talarurus (Carpenter, 2004) but the olfactory tract was located more posteriorly, well within the endocranial cavity.
In UALVP 47977, a conspicuous descending process fused to the ventral surface of the frontal develops at the front of the olfactory fenestra. The descending process accommodates a deep, spacious groove that originates from the anterior margin of the orbit. Its anterolateral site of origin is associated with vascular impressions on the medial surface of the lacrimal. The groove extends medially along the anterior wall of the olfactory region and then posteriorly along the lateral wall of the main airway, and finally ventrally along the descending process. A deep sulcus parallels the groove medially along the lateral wall of the main airway. The soft tissue that filled this groove was extensively vascularized because of the vascular impressions at the anterolateral end of the groove and because of the sulcus associated with the groove along the lateral wall of the main airway.
In another skull of Euoplocephalus (AMNH 5405), a tunnel extends anterolaterally within the roof of the olfactory region (Fig. 4) and presumably opens into the descending process. Witmer & Ridgely (2008) did not reconstruct this tunnel in AMNH 5405, but it is present on both sides in their CT data. A re-examination of the CT slices revealed that the tunnel branches laterally. Although UALVP 47977 does not have the tunnel, the vascular impression associated with the groove in the olfactory region suggests that at least the vascular component of the tissue filling the groove may correspond to the tissue filling the tunnel in AMNH 5405. The descending process and the groove could not be reconstructed from the CT scan of UALVP 31 (Fig. 5). UALVP 47977 has cracks that show the cross-sections of the frontal and the nasal. None of these cross-sections indicate pneumatization within the bones.
Figure 4. Sagittal sections of a Euoplocephalus skull (AMNH 5405) from CT data of Witmer & Ridgely (2008) show a tunnel within the frontal bone, laterally positioned and passing medially and slightly posteriorly on both sides. The most lateral sagittal section for each side is where the canal disappears into the bone. Arrowhead indicates the tunnel within the frontal, and letters A–H indicate the levels of the CT slices on the skull. Anterior is to the right in all CT slices and in the 3D model of the skull. CT data are available from the website (http://www.oucom.ohiou.edu/dbms-witmer/3D-Visualization.htm).
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Figure 5. CT-based reconstruction corroborates direct osteological observation. CT renderings of the skull roofs of two Euoplocephalus specimens, AMNH 5405 (A,C) and UALVP 31 (B,D). A and B show in dark grey the portion of the skull represented in C and D in relation to the entire skull, in oblique right anterior view. C and D are sliced to mimic the areas preserved in UALVP 47977, and show internal features of the skull in ventral view that correspond to those of UALVP 47977 (Fig. 2), with anterior towards the bottom of the page. oo, ocular osteoderm; pp, paroccipital process; q, quadrate. For other abbreviations, see Figs 1 and 2.
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UALVP 47977 preserves the mesethmoid, the sphenethmoid and the ectethmoid, all of which are fully mineralized (Figs 2 and 7). The mesethmoid is a septum on the midline that separated the olfactory bulbs and is continuous anteriorly with the mineralized nasal septum. The sphenethmoid is the lateral element of the ethmoidal complex (generally referred to as a presphenoid in ornithischians: Horner, 1992; Evans, 2005, 2006) that enveloped the olfactory bulb ventrally and laterally. The sphenethmoid is continuous with the lateral wall of the main airway. The mineralized median septum of the olfactory bulbs has been described for a variety of non-avian theropods (Brochu, 2002; Coria & Currie, 2002; Sampson & Witmer, 2007; Ali et al. 2008) and is considered a homologue of the mesethmoid in birds (Ali et al. 2008). Following this position, the ossified median septum of the ethmoidal complex in UALVP 47977 is identified as the mesethmoid. It is not possible to distinguish the boundary between the mesethmoid and the sphenethmoid in UALVP 47977 and these two elements probably fused to each other early in ontogeny.
The ectethmoid forms a thin lateral wall of the olfactory region, separating it from the orbital depression laterally. It contacts the orbitosphenoid posteriorly and the lacrimal anteriorly, although the sutures are not visible at either end. Because of the skull width and the relatively more anterior placement of the orbit, the ectethmoid is elongate and oriented anterolaterally rather than transversely. The ectethmoid forms a small, medially overhanging shelf near the base of the descending process. A small foramen that pierces the ectethmoid on the left side of the skull from the orbital depression to the olfactory region may represent the orbitonasal foramen.
Anteriorly to the ethmoidal complex, the nasal septum and the lateral walls of the main airway are mineralized (Figs 2 and 3). There is no suture that distinguishes the mineralized septum and walls of the main airway from any of the cranial elements, including the ethmoidal complex, nasal, frontal and lacrimal, which they contact. The nasal septum and the lateral walls converge at the midline anterior to the ethmoidal complex. There is no opening that connects the dorsomedial passage of the main airway with the endocranial cavity. The skull roof is damaged and does not preserve the ventral part of the main airway. On the right side of the skull, however, the preserved part of the lateral wall extends ventromedially. This suggests that the mineralized wall wrapped around the dorsomedial passage of the main airway ventrally as well as laterally and medially. The anterior wall of the olfactory region extends lateromedially between the lateral wall of the main airway and the lacrimal. The anterior wall separates the olfactory region and the groove filled with the vascularized tissue from the cavity that housed the posterior loop of the main airway anteriorly (Witmer & Ridgely, 2008).
The orbitosphenoid contacts the ectethmoid anterolaterally and the ethmoidal complex (sphenethmoid + mesethmoid) anteriorly (Figs 2 and 7). The olfactory fenestra opens between these two contacts. The olfactory nerves (CN I) would have diffused from this fenestra to both lateral and medial sides of the descending process. The orbitosphenoid contacts the laterosphenoid posteriorly and the parasphenoid ventrally. The laterosphenoid is short anteroposteriorly, but has a long, laterally oriented postorbital process that is approximately half the width of the transversely expanded ankylosaurid skull. The element is firmly fused to the skull roof. Two other sets of foramina pierce the orbitosphenoid. The foramen for the optic nerve (CN II) is larger than all other foramina for the cranial nerves except the olfactory fenestra and consists of a single exit (Fig. 7). The shared foramen for the oculomotor (CN III) and trochlear (CN IV) nerves opens posterior to the optic foramen. The foramen for the abducens nerve (CN VI) opens directly ventral to the oculomotor/trochlear foramen, which is consistent with these foramina transmitting motor nerves to the extraocular muscles.
In the laterosphenoid, the foramen for the trigeminal nerve (CN V) is posterior to the oculomotor/trochlear foramen. Just dorsal to the trigeminal foramen is an aperture for the anterior middle cerebral vein. The trigeminal foramen is anteroventral with respect to the lateral wing of the braincase (pila antotica) that contacts the postorbital laterally. In addition, the trigeminal nerve is associated with the prootic in sauropsids. Although no suture can be observed between the laterosphenoid and prootic, the topographical relationships of the trigeminal foramen with other braincase landmarks suggest that the foramen was mainly within the laterosphenoid with contribution from the prootic posteriorly. This implies that the prootic extended anteriorly below the lateral wing of the laterosphenoid. This interpretation is supported by the location of the foramen for the facial nerve (CN VII), which is located completely within the prootic in sauropsids and is just posteroventral to the trigeminal foramen.
The description of the cranial endocasts focuses on AMNH 5405, which has the best preserved braincase amongst the specimens used in this study. The newly prepared cranial endocasts (AMNH 5405, UALVP 31 and UALVP 47977; Fig. 7) compare well with the published description of the cranial endocast of AMNH 5337 (Coombs, 1978a). In all specimens, the brains were anteroposteriorly short but relatively straight. The cranial endocast of UALVP 31 has a blockier, more robust appearance than that of AMNH 5405, because of the lower resolution of the CT data for UALVP 31. The endocast is also more strongly bowed dorsoventrally compared to the other specimens, but this is probably a result of taphonomic distortion of the skull. The anteroposterior shortening of the olfactory stalk partly accounts for the short anteroposterior length of the cranial endocasts of Euoplocephalus. The anteroposterior distance between the olfactory fenestra and the root of the optic nerve is less than a quarter the entire anteroposterior length of the cranial endocast in Euoplocephalus, whereas the distance is typically more than a third the length of the cranial endocast in other dinosaurs (based on figures in Hopson, 1979; Brochu, 2002; Sampson & Witmer, 2007; Witmer et al. 2008).
Figure 7. Comparison of cranial endocasts and that of braincases reveals minor variation amongst specimens referred to as Euoplocephalus. The braincase of AMNH 5405 in left lateral view (A), the cranial endocast of the same specimen in left lateral (B), dorsal (C) and ventral (D) views, the braincase of UALVP 47977 in right lateral view (E), the cranial endocast of the same specimen in right lateral (F) and ventral (G) views, and the cranial endocast of UALVP 31 in right lateral (H) and ventral (I) views. The images E–I were all inverted horizontally to show the right sides in the same orientation with the left side of AMNH 5405 for the purpose of comparison. In both UALVP 47977 and UALVP 31, the right side is better preserved. UALVP 47977 is represented by a line drawing of a latex cast, and AMNH 5405 and UALVP 31 are 3D models based on CT data. Roman numerals refer to either the foramen for, or the trunk of, the cranial nerve. amcv, anterior middle cerebral vein; amp, insertion site for M. adductor mandibulae posterior; sensuHolliday & Witmer, 2007; fl, flocculus; fv, fenestra vestibularis; ic, internal carotid artery; ocv, orbitocerebral vein; of, olfactory fenestra; pmcv, posterior middle cerebral vein; sp, sinus of pituitary. For other abbreviations, see Figs 1 and 2.
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The olfactory bulbs diverge immediately anterior to the cerebrum at an angle of 80–100º and lead to the olfactory fenestra opening at the posteromedial end of the olfactory region. A general condition for ornithischian dinosaurs is that the olfactory tracts did not diverge as strongly anterolaterally as in Euoplocephalus (Hopson, 1979; Galton, 1983, 1988, 1989, 1997, 2001; Evans et al. 2009). The cerebral hemispheres are fairly discrete on the endocast, forming a rounded swelling immediately posterior to the olfactory tract. As is often the case in non-coelurosaurian dinosaurs (Witmer & Ridgely, 2009), however, other major neural structures such as the optics lobes and cerebellum are largely obscured by the dural envelope. An important exception is the flocculus (cerebellar auricle). The flocculus on the endocast of AMNH 5405 extends posterolaterally as a substantial, finger-like projection into the region of the inner ear and breaks the plane of the anterior semicircular canal. The presence of a flocculus in AMNH 5405 clears up the discrepancy in the reports on AMNH 5337 between Coombs (1978a: no flocculus) and Hopson (1979: large flocculus) in favor of the latter interpretation. The structure interpreted as an epiphysis cerebri (= pineal gland) projecting from the diencephalon noted in AMNH 5337 by Coombs (1978a) is also present in the endocasts of UALVP 31 and AMNH 5405, but is not visible in the endocast of UALVP 47977. Although being small, this structure is in the position to be the epiphysis. Epiphyses are present in extant birds and have been reconstructed in some dinosaurs (e.g. some theropods; Witmer & Ridgely, 2009). The lack of the epiphysis in UALVP 47977 is probably due to the presence of plaster infilling, which was used to strengthen the cracks during preparation of this specimen.
As already noted in the braincase description, the optic nerves in the endocast project almost directly laterally, such that the optic chiasm is oriented transversely rather than anterolaterally as in other archosaurs. The shared exit for the oculomotor and trochlear nerves is a large trunk directly posterior to the optic nerve. Both Coombs (1978a) and Hopson (1979) interpreted the smaller twig dorsal to the definitive oculomotor nerve canal as the trochlear nerve. This interpretation was widely accepted in the subsequent ankylosaur literature and the corresponding foramen was identified as that for the trochlear nerve in Amtosaurus (Averianov, 2002), Saichania (Maryańska, 1977), Sauropelta and Tatankacephalus (Parsons & Parsons, 2009). We instead regard their putative trochlear nerve as an orbitocerebral vein. In the endocast of AMNH 5405, the ‘trochlear nerve’ of Coombs (1978a) and Hopson (1979) is comparable to the orbitocerebral vein canals of sauropods (Sereno et al. 2007; Witmer et al. 2008), theropods (Sampson & Witmer, 2007; Witmer & Ridgely, 2009) and other dinosaurs. This feature in AMNH 5405 emerges from the lateral pole of the cerebral region and opens into the orbit well dorsal to the canals for the other nerves supplying the extraocular muscles.
The trunk of the oculomotor nerve in this study was identified by Coombs (1978a) as being associated with the pituitary vein. Indeed, this canal shared by the trochlear and oculomotor nerves seems too large to have transmitted only these two small nerves. It is likely that veins also traversed this canal. However, the term ‘pituitary vein’ is not appropriate because the venous drainage of the pituitary was almost certainly within the pituitary fossa itself and the cavernous sinus within (see Sampson & Witmer, 2007). The trunk of the abducens nerve originates from the ventral side of the brain below the trigeminal nerve and passes anterolaterally below the oculomotor and trochlear nerves.
The fossa for the pituitary gland projects more or less straight ventrally in all the specimens as a bulbous structure. In AMNH 5405, the bulbous structure is twice as wide transversely as long anteroposteriorly. Ventral to the pituitary, the endocast of the internal carotid artery is oriented ventrolaterally, whereas the artery extended anterodorsally in the cranial endocasts of other dinosaurs (Hopson, 1979; Witmer et al. 2008). The pituitary in UALVP 31 expands posteriorly, but this is most likely a result of damage to the ventral portions of the braincase. The pituitary fossa of AMNH 5405 also preserves large paired apertures dorsal to the carotid canals, which almost certainly transmitted the sphenoid branch of the carotid artery into the floor of the orbit as well as receiving ophthalmic veins.
The single trunk of the trigeminal nerve indicates that the branches diverged outside the endocranial cavity. The endocast of this nerve is dorsoventrally taller than anteroposteriorly long, suggesting that the canal housed the ganglion, as in most dinosaurs except for tyrannosaurids and birds (Witmer et al. 2008). The anterior middle cerebral vein is preserved above the trigeminal nerve in the cranial endocast of AMNH 5405 (Fig. 7C). The trunk of the facial nerve originated from the shallow recess shared with that of the vestibulocochlear nerve (CN VIII). The course of the facial nerve closely parallels that of the trigeminal nerve anteriorly and laterally, and diverges away from that of the vestibulocochlear nerve. The trunk of the vestibulocochlear nerve has two branches that separate from each other immediately outside the endocranial cavity. The dorsal branch is directed laterally toward the vestibule and the ventral one toward the cochlear ventrally. The trunks of the glossopharyngeal, vagus and accessory nerves (CNs IX–XI) exit the endocranial cavity through the jugular foramen. The jugular foramen is directly anterior to the foramen for the posterior branch of the hypoglossal nerve. AMNH 5405 has two trunks for the hypoglossal nerve, although there are possibly three trunks for this nerve in AMNH 5337 (Coombs, 1978a) and UALVP 47977 (Fig. 7). Even in the case of three trunks, the proximity and directions of the two smaller anterior trunks suggest that they likely joined to emerge from a single external foramen. In AMNH 5405, the foramen for the anterior trunk of the hypoglossal nerve is merged to the posteroventral corner of the jugular foramen. The foramen for the larger posterior trunk opens directly posterior to the jugular foramen on the lateral surface of the base of the occipital condyle.
The labyrinth of the inner ear is reasonably well preserved on the left side of AMNH 5405 and is generally similar to the one illustrated for AMNH 5337 by Hopson (1979). The lateral semicircular canal is extremely reduced, more so than in perhaps any dinosaur described to date. The anterior canal may seem somewhat elongate but this may result more from the constraint that the anterior canal must pass around the flocculus (Witmer et al. 2003). The cochlea is remarkably elongate in AMNH 5405, as illustrated also for AMNH 5337 by Hopson (1979). The elongate cochlea suggests that hearing was an important sense in Euoplocephalus.