Odontopteryx toliapica, Owen, 1873

Milner, Angela C. & Walsh, Stig A., 2009, Avian brain evolution: new data from Palaeogene birds (Lower Eocene) from England, Zoological Journal of the Linnean Society 155 (1), pp. 198-219 : 202-205

ODONTOPTERYX TOLIAPICA

It has been possible to reconstruct almost the entire endocranial cast of Odontopteryx , including pathways of major efferent and afferent nerves, and the arrangement of the anastomosis intercarotica (see Table 1 for measurements). Both osseous labyrinths are largely intact, and were reconstructed fully on each side. However, no evidence of the columella was detected within the recessus antivestibularis. Using the position of the canalis semicircularis horizontalis in the skull ( Pearson, 1972) it has been possible to determine the in vivo alert head posture of Odontopteryx , and this is shown in Figure 2A. A detailed description of the osteology of O. toliapica can be found in Harrison & Walker (1976a). As with living avian taxa, the major cranial bones of the braincase are fused. However, the CT reconstruction shows that the frontals overlap the parietals caudally, and at the posterior region of the frontals the two bones are unfused. A faint outline within the matrix covering left side of BMNH 44096 is interpreted to correspond broadly to the shape of the tractus opticus ( Fig. 3C ), but it was not possible to reconstruct the feature on the right side where the matrix was absent. Including cranial nerves but excluding the carotid rami the total endocranial volume of Odontopteryx is 9.05 mL.

As in most living birds, the brain of Odontopteryx was equant in dorsal view, with the distance from the caudal-most extent of the cerebellum to the rostralmost extent of the bulbus olfactorius almost exactly equalling that measured for the telencephalic width (31.5 mm). Also as in all extant birds the tectum mesencephali (optic lobes) are largely occluded in dorsal view by the lateral expansion of the telencephalon ( Fig. 3A ); in Archaeopteryx the tectum mesencephali extend as far laterally as the telencephalon ( Domínguez et al., 2004).

The bulbus olfactorius is relatively large and elongate, approaching the proportions of the same region in many Anseriformes (e.g. Branta , Aix ) and some Charadriiformes (e.g. Burhinus , Sterna ), and far larger than in taxa with well-developed optical specializations such as Strigiformes . The bulbus apparently did not bifurcate until the nerve bundles entered the tractus olfactorius, nor is there any indication of the development of a rostrocaudally All values were measured at maximum orthogonal points, and are in millimetres. Note that semicircular canal length measurements refer to maximum dorsal (for csr) and lateral (for csh and csc) extent of canal arc; width measurements refer to maximum canal diameter. See text for abbreviations.

directed sulcus in the dorsal surface of the bulb ( Fig. 3B, C ). In most Charadriiformes , Ciconiiformes , and Pelecaniformes this groove is present in the dorsal surface of the bulbus, and in many Coraciiformes, Caprimulgiformes , and Psittaciformes the bifurcation occurs internally, such that the tractus olfactorius emerges as two separate branches from the rostral region of the brain. The bulbus olfactorius also occupies a position close to the dorsal surface of the telencephalon as in Charadriiformes and Coraciiformes . In Pelecaniformes and taxa possessing a well-developed rostrally positioned eminentia sagittalis (especially Strigiformes ) the bulbus is positioned far more ventrally.

In dorsal view, the two telencephalic hemispheres form a spade shape, with a marked expansion of the lateral regions ( Fig. 3B ). As a result of this expansion the rostral edge of the telencephalon is slightly notched in this view. A narrow and very poorly developed eminentia sagittalis is present in a rostral position ( Figs 3A, B , 4A ). The feature is only very slightly raised, and remains constant in width as it extends from a point slightly caudal of the rostral margin of the telencephalon to 8 mm rostral of the point where the telencephalon meets the cerebellum. No evidence of a vallecula is detectable. The eminentia sagittalis of Odontopteryx appears to be most similar to that of some Coraciiformes , and unlike any pelecaniform for which we have comparative data.

The cerebellum is short (46% of the total brain length as measured along the interhemispheric fissure) and broad (42% of the maximum telencephalic width). The auricula cerebelli are large, expand distally and extend ventrocaudally from the ventral margin of the cerebellum ( Figs 3A, C , 4B ). Except for at the junction of the tectum mesencephali and cerebellum ventral of the protruberantia tentorialis on the left-hand side of the brain, there is no trace of the vena semicircularis rostralis ( Fig. 3C ), and the vein was apparently fully enclosed within an osseous tunnel. There is also no evidence of a median groove for the sinus occipitalis, although slight compression of the parietal region may mask its presence.

Although the reconstruction of the left side of the tractus opticus is by no means certain, it suggests that the optic nerve extended some way from the tectum mesencephali before bifurcating ( Fig. 3C ). The length of the tractus opticus is apparently variable in most avian orders, but in some (e.g. Strigiformes, Caprimulgiformes , some Psittaciformes , Apteryx ) the two optic nerves separate close to, or within the tectum mesencephali. This arrangement appears to be most common in taxa with high angles between the brain and bill axes, and perhaps relates to the reduced distance between the tectum mesencephali and orbits in these species (e.g. in owls and parrots).

The tectum mesencephali itself is large and globelike, but appears distinctly lunate in lateral view because of interpenetration of the telencephalic hemispheres ( Fig. 3C ). In other taxa (e.g. Columba ) the tectum mesencephali is dorsoventrally compressed into a distinct oval, which may or may not be penetrated dorsally by the telencephalon. A rounded junction with the telencephalon is seen in several species (e.g. Larus , Pelecanus , Phalacrocorax ), although a straight or angular junction is also common (e.g. Pluvialis , Sterna ).

The hypophysis is rostrocaudally short and is smaller than the tractus opticus ( Fig. 4B ). The body of the hypophysis is only slightly laterally compressed and has a rounded ventral margin of the pars distalis that is unlike that of Anseriformes , where the pars distalis is flattened and elongate ( Wingstrand, 1951). The rostral region of the pars distalis is markedly conical ( Fig. 4B ), a feature that may relate to presence of an epithelial stalk. Although our reconstruction ( Fig. 4B ) shows no gap between the hypophysis and rhombencephalon, a thin dorsum sellae is present that separates the regions, as in most large species of modern birds ( Wingstrand, 1951). The bony tunnel that housed the ascending portion of the carotid artery terminates at the caudal-most edge of the base of the hypophysis. The tunnel is broad at this point, and widens as it extends rostroventally from the hypophysis, before bifurcating. The two separate tunnels then curve sharply and extend caudolaterally as they follow the line of the basisphenoid. The tunnel on the right-hand side can be traced caudally for 8.4 mm, but the path of the left-hand tunnel is difficult to discern as a result of replacement by pyrite. Because the bifurcation of the cranial ramus of the artery (dorsal of the hypophysis) must have occurred within the sella turcica, it is not possible to determine the exact pattern of anastomosis in Odontopteryx . However, the regions that can be examined are similar to those seen in Pelecanus , although the enlarged sphenomaxillary and palatine arteries found in that genus (see Baumel & Gerchman, 1968) are absent.

The rhombencephalon ( Fig. 4B ) is globe-shaped and extends from the foramen magnum to around the midpoint of the mesencephalon. The base of the rhombencephalon shows no evidence of a ventral sulcus. On the left-hand side of the rhombencephalon a wide n. trochlearis is visible extending rostrally, but on the right-hand side only the base of the nerve can be detected. A faint trace of the n. occulomotorius is detectable on the left-hand side, extending rostrodorsally from the dorsal region of the hypophysis to the tractus opticus. The n. trigeminus is particularly broad and its exit from the rhombencephalon is contiguous with the ventral margin of the tectum mesencephali. The n. cochlearis and n. facialis are preserved as a low dorsoventrally compressed protuberance positioned immediately caudal and slightly more ventral of the n. trigeminus. The n. vagus and n. glossopharyngeus also exit the rhombencephalon together and combined are as broad as the n. trigeminus, although slightly dorsoventrally compressed. The n. glossopharyngeus diverges from the n. vagus to exit the skull within the recessus scalae tympani slightly medial of the exit of the n. vagus. As the n. vagus/n. glossopharyngeus exit the rhombencephalon the nerve bundle is directed ventrolaterally, but curves dorsally as the smaller ventrolaterally directed n. hypoglossus branches from it. No traces of the n. accessorius are visible in this region.

An impression of the bony labyrinth of the inner ear is visible on the endocast of the cerebellum ( Fig. 3C ). The canals of the labyrinth itself are comparatively short and broad ( Fig. 5A–C ), with welldefined ampullae. The labyrinth is separated from the telencephalon by the tectum mesencephali and a protruberantia tentorialis. The rostral limb of the canalis semicircularis rostralis slopes caudally as it rises from the ampulla ossea rostralis, smoothly curving round and back until it is directed rostrally before its junction with the canalis semicircularis caudalis. The canalis semicircularis rostralis is tall, representing 50% of the total dorsoventral height of the labyrinth. The caudal limb of the canalis semicircularis rostralis frames the foramen magnum, and therefore the canalis semicircularis rostralis of each side do not come close to meeting caudally as they do in Turdus . The long axis of the canalis semicircularis rostralis is angled laterally at 85° (mean of rostral and caudal measurements for both sides), and in dorsal view exhibits a slight sigmoidal curvature. The canalis semicircularis rostralis et caudalis cross at a mean angle of 49° to each other. The canalis semicircularis caudalis et horizontalis meet at 82°. The ductus cochlearis is straight, directed strongly rostrally and slightly medially, and is approximately round in section. The fenestra cochlearis is small and faces caudolaterally, and slightly ventrally. The position of the oval window for the columella is marked by the medial extent of the small and dorsoventrally compressed recessus antivestibularis. A well-developed dorsoventrally compressed sacculus is present on the lateral surface of the ductus cochlearis.

Figures

Figure 2. Transparent computed tomographic (CT) segmentation of two Lower Eocene skulls in right lateral views, revealing the virtual endocasts of the brain and osseous labyrinth. Compare positions of the canalis semicircularis horizontali indicating the in vivo alert head positions. A, Odontopteryx toliapica; all sutures are fully obliterated except that between the frontals and parietals. B, Prophaethon shrubsolei.

Figure 3. Virtual endocast of Odontopteryx toliapica in A, dorsal; B, rostral, and C, left lateral views. See text for list of anatomical abbreviations.

Figure 4. Virtual endocranial cast of Odontopteryx toliapica. A, expanded view of the dorsal surface of the telencephalon, showing the shape and extent of the poorly developed eminentia sagittalis. B, ventral view of virtual endocast. See text for list of anatomical abbreviations.

Figure 5. Reconstruction of the left osseous labyrinth of Odontopteryx toliapica in A, rostral; B, lateral; C, caudal, and D, medial views. See text for list of anatomical abbreviations.