A proxy for brain-to-endocranial cavity index in non-neornithean dinosaurs and other extinct archosaurs.

Although the brain fills nearly the entire cranial cavity in birds, it can occupy a small portion of it in crocodilians. The lack of data regarding the volumetric correspondence between the brain and the cranial cavity hampers thorough assessments of the degree of encephalization in non-neornithean dinosaurs and other extinct archosaurs and, consequently, informed inferences regarding their cognitive capacities. Existing data suggest that, across extant archosaurs, the degree of endocranial doming and the volume of intracranial nonneural components are inversely related. We build upon this information to develop an equation relating these two anatomical features in non-neornithean dinosaurs and other extinct archosaurs. We rely on measurements of the endocast doming and brain-to-endocranial cavity (BEC) index in extant relatives of non-neornithean dinosaurs, namely, the crurotarsans Caiman crocodilus, Crocodylus niloticus, and Crocodylus porosus; the paleognaths Struthio camelus and Apteryx mantelli; and the fowl Macrocephalon maleo, Gallus gallus, Meleagris gallopavo, Phasianus colchicus, and Anas platyrhynchos. Applying the equation to representative endocasts from major clades of dinosaurs, we found that BEC varies from about 0.6 in ceratopsians and thyreophorans to around 0.7 in ornithopods, pachycephalosaurians, sauropods, and theropods. We, therefore, warn against the use of a catch-all value, like 0.5, and instead encourage refinement in the adoption of BEC across archosaurs.

New theropod dinosaur from the Lower Cretaceous of Japan provides critical implications for the early evolution of ornithomimosaurs.

Ornithomimosauria consists of the ostrich-mimic dinosaurs, most of which showing cursorial adaptations, that often exhibit features indicative of herbivory. Recent discoveries have greatly improved our knowledge of their evolutionary history, including the divergence into Ornithomimidae and Deinocheiridae in the Early Cretaceous, but the early part of their history remains obscured because their fossil remains are scarce in the Aptian-Albian sediments. In recent years, many isolated ornithomimosaur remains have been recovered from the Aptian Kitadani Formation of Fukui, central Japan. These remains represent multiple individuals that share some morphological features common to them but unknown in other ornithomimosaurs, suggesting a monospecific accumulation of a new taxon. As a result of the description and phylogenetic analysis, the Kitadani ornithomimosaur is recovered as a new genus and species Tyrannomimus fukuiensis, the earliest definitive deinocheirid that complements our knowledge to understand the early evolutionary history of Ornithomimosauria. Due to its osteological similarity to Tyrannomimus, a taxon previously considered an early tyrannosauroid based on fragmentary specimens, namely Aviatyrannis jurassica, may represent the earliest ornithomimosaur from the Upper Jurassic of Europe, significantly expanding the temporal and biogeographic range of Ornithomimosauria. This finding fills a 20-million-year ghost lineage of Ornithomimosauria implied by the presence of the oldest fossil record of Maniraptora from the Middle Jurassic and is consistent with the hypothesis that their biogeographic range was widespread before the Pangaean breakup in the Kimmeridgian.

Anatomical network analyses reveal evolutionary integration and modularity in the lizards skull.

The morphology of lizard skulls is highly diverse, and it is crucial to understand the factors that constrain and promote their evolution to understand how lizards thrive. The results of interactions between cranial bones reflecting these factors can be detected as integration and modularity, and the analysis of integration and modularity allows us to explore the underlying factors. In this study, the integration and modularity of the skulls of lizards and the outgroup tuatara are analyzed using a new method, Anatomical Network Analysis (AnNA), and the factors causing lizards morphological diversity are investigated by comparing them. The comparison of modular structures shows that lizard skulls have high integration and anisomerism, some differences but basically common modular patterns. In contrast, the tuatara shows a different modular pattern from lizards. In addition, the presence of the postorbital bar by jugal and postorbital (postorbitofrontal) also reflect various functional factors by maintaining low integration. The maintenance of basic structures due to basic functional requirements and changes in integration within the modules play a significant role in increasing the morphological diversity of the lizard skull and in the prosperity of the lizards.

Palaeoneurology of the early cretaceous iguanodont Proa valdearinnoensis and its bearing on the parallel developments of cognitive abilities in theropod and ornithopod dinosaurs.

Proa valdearinnoensis is a relatively large-headed and stocky iguanodontian dinosaur from the latest Early Cretaceous of Spain. Its braincase is known from three specimens. Similar to that of other dinosaurs, it shows a mosaic ossification pattern in which most of the bones seem to have fused together indistinguishably while a few (frontoparietal, basioccipital) might have remained loosely attached. The endocasts of the three specimens are described based on CT data and digital reconstructions. They show unmistakable morphological similarities with the endocast of closely related taxa, such as Sirindhorna khoratensis (which is close in age but from Thailand). This supports a high conservatism of the endocranial cavity. The issue of volumetric correspondence between endocranial cavity and brain in dinosaurs is analyzed. Although a brain-to-endocranial cavity (BEC) index of 0.50 has been traditionally used, we employ instead 0.73. This is indeed the mid-value between the situation in adults of Alligator mississippiensis and Gallus gallus, which are members of the extant bracketing taxa of dinosaurs (Crocodilia and Aves). We thence gauge the level of encephalization of P. valdearinnoensis through the calculation of the encephalization quotient (EQ), which remains valuable as a metric for assessing the degree of cognitive function in extinct taxa, especially those with fully ossified braincases like dinosaurs and other archosaurs. The EQ obtained for P. valdearinnoensis (3.611) suggests that this species was significantly more encephalized than most if not all extant nonavian, nonmammalian amniotes. Our work adds to the growing body of data concerning theoretical cognitive capabilities in dinosaurs and supports the idea that an increasing encephalization was fostered not only in theropods but also in parallel in the shorter-lived lineage of ornithopods. P. valdearinnoensis was ill-equipped to respond to theropod dinosaurs and possibly lived in groups as a strategy to mitigate the risk of being predated upon. We hypothesize that group-living and protracted caring of juveniles in this and possibly many other iguanodontian ornithopods favored a degree of encephalization that was outstanding by reptile standards.

The so-called foramen singulare in cetacean periotics is actually the superior vestibular area.

It is nearly 100 years ago that the "foramen singulare" was first identified in cetacean periotics. Since then, the "foramen singulare" has been recognized in periotics of many cetacean species, extant or extinct. Surprisingly, however, it has never been confirmed if the foramen singulare in cetacean periotics is really homologous to that in other mammals. It is known that in mammals including humans the posterior ampullary nerve, which innervates the posterior semicircular duct, passes through the foramen singulare. We use an X-ray micro-CT scan to examine endocasts of the bony labyrinth of the inner ear of cetacean periotics, showing that the osseous canal extending from the so-called foramen singulare goes toward the anterior bony ampulla, meaning that the alleged foramen singulare in cetacean periotics is really the superior vestibular area, through which the utriculoampullary nerve enters. The transverse crest is quite significant to identify each quadrant of the fundus of the internal acoustic meatus, but in many cetacean species the transverse crest is poorly developed, almost imperceptible in some species, and this could have brought confusion into the interpretation over the superior vestibular area and the foramen singulare. The bony septum separating the cerebral aperture of the facial canal from the foramen singulare is not the transverse crest, but the perpendicular crest. The foramen singulare is not a distinct foramen separated from the inferior vestibular area. Instead, the true foramen singulare opens near the inferior vestibular area in the internal acoustic meatus in cetacean periotics.

Endocranial anatomy of the ceratopsid dinosaur Triceratops and interpretations of sensory and motor function.

Triceratops is one of the well-known Cretaceous ceratopsian dinosaurs. The ecology of Triceratops has been controversial because of its unique morphological features. However, arguments based on brain and inner ear structures have been scarce. In this study, two braincases (FPDM-V-9677 and FPDM-V-9775) were analyzed with computed tomography to generate three-dimensional virtual renderings of the endocasts of the cranial cavities and bony labyrinths. Quantitative analysis, including comparison of linear measurements of the degree of development of the olfactory bulb and inner ear, was performed on these virtual endocasts to acquire detailed neuroanatomical information. When compared with other dinosaurs, the olfactory bulb of Triceratops is relatively small, indicating that Triceratops had a reduced acuity in sense of smell. The lateral semicircular canal reveals that the basicranial axis of Triceratops is approximately 45° to the ground, which is an effective angle to display their horns as well as frill, and to graze. The semicircular canals of Triceratops are relatively smaller than those of primitive ceratopsians, such as Psittacosaurus and Protoceratops, suggesting that sensory input for the reflexive stabilization of gaze and posture of Triceratops was less developed than that of primitive ceratopsians. The cochlear length of Triceratops is relatively short when compared with other dinosaurs. Because cochlear length correlates with hearing frequency, Triceratops was likely adapted to hearing low frequencies.

Tempo and Pattern of Avian Brain Size Evolution.

Relative brain sizes in birds can rival those of primates, but large-scale patterns and drivers of avian brain evolution remain elusive. Here, we explore the evolution of the fundamental brain-body scaling relationship across the origin and evolution of birds. Using a comprehensive dataset sampling> 2,000 modern birds, fossil birds, and theropod dinosaurs, we infer patterns of brain-body co-variation in deep time. Our study confirms that no significant increase in relative brain size accompanied the trend toward miniaturization or evolution of flight during the theropod-bird transition. Critically, however, theropods and basal birds show weaker integration between brain size and body size, allowing for rapid changes in the brain-body relationship that set the stage for dramatic shifts in early crown birds. We infer that major shifts occurred rapidly in the aftermath of the Cretaceous-Paleogene mass extinction within Neoaves, in which multiple clades achieved higher relative brain sizes because of a reduction in body size. Parrots and corvids achieved the largest brains observed in birds via markedly different patterns. Parrots primarily reduced their body size, whereas corvids increased body and brain size simultaneously (with rates of brain size evolution outpacing rates of body size evolution). Collectively, these patterns suggest that an early adaptive radiation in brain size laid the foundation for subsequent selection and stabilization.

Avian palaeoneurology: Reflections on the eve of its 200th anniversary.

In birds, the brain (especially the telencephalon) is remarkably developed, both in relative volume and complexity. Unlike in most early-branching sauropsids, the adults of birds and other archosaurs have a well-ossified neurocranium. In contrast to the situation in most of their reptilian relatives but similar to what can be seen in mammals, the brains of birds fit closely to the endocranial cavity so that their major external features are reflected in the endocasts. This makes birds a highly suitable group for palaeoneurological investigations. The first observation about the brain in a long-extinct bird was made in the first quarter of the 19th century. However, it was not until the 2000s and the application of modern imaging technologies that avian palaeoneurology really took off. Understanding how the mode of life is reflected in the external morphology of the brains of birds is but one of several future directions in which avian palaeoneurological research may extend. Although the number of fossil specimens suitable for palaeoneurological explorations is considerably smaller in birds than in mammals and will very likely remain so, the coming years will certainly witness a momentous strengthening of this rapidly growing field of research at the overlap between ornithology, palaeontology, evolutionary biology and neurosciences.

An unusual bird (Theropoda, Avialae) from the Early Cretaceous of Japan suggests complex evolutionary history of basal birds.

The Early Cretaceous basal birds were known largely from just two-dimensionally preserved specimens from north-eastern China (Jehol Biota), which has hindered our understanding of the early evolution of birds. Here, we present a three-dimensionally-preserved skeleton (FPDM-V-9769) of a basal bird from the Early Cretaceous of Fukui, central Japan. Unique features in the pygostyle and humerus allow the assignment of FPDM-V-9769 to a new taxon, Fukuipteryx prima. FPDM-V-9769 exhibits a set of features comparable to that of other basalmost birds including Archaeopteryx. Osteohistological analyses indicate that FPDM-V-9769 is subadult. Phylogenetic analyses resolve F. prima as a non-ornithothoracine avialan basal to Jeholornis and outgroup of the Pygostylia. This phylogenetic result may imply a complex evolutionary history of basal birds. To our knowledge, FPDM-V-9769 represents the first record of the Early Cretaceous non-ornithothoracine avialan outside of the Jehol Biota and increases our understanding of their diversity and distribution during the time.

The sandwich structure of keratinous layers controls the form and growth orientation of chicken rhinotheca.

The upper beak bone of birds is known to be overlain by the rhinotheca, which is composed of the horny sheath of keratinous layers. However, the details of the structure and growth pattern of the rhinotheca are yet to be understood. In this study, the microstructure of the rhinotheca from chicken specimens of different growth stages (ranging from 1 to ~ 80 days old) was analyzed using a combination of thin section and scanning electron microscopy observations, and small-angle X-ray scattering analysis. We found that the rhinotheca comprises three different layers - outer, intermediate, and inner layers - throughout its growth. The outer layer arises from the proximal portion of the beak bone and covers the dorsal surface of the rhinotheca, whereas the intermediate and inner layers originate in the distal portion of the beak bone and underlie the outer layer. This tri-layered structure of the rhinotheca was also observed in wild bird specimens (grey wagtail, king quail, and brown dipper). On the median plane, micro-layers making up the outer and inner layers are bedded nearly parallel to the rostral bone at the base. However, more distally positioned micro-layers of the outer layer are more anteverted distally. The micro-layers of the intermediate layer are bedded nearly perpendicular to those of the outer and inner layers on the median plane. The growth of micro-layers in the intermediate layer adds thickness to the rhinotheca, which causes the difference in profile between the beak bone and the rhinotheca in the distal portion of the beak. Moreover, the entire intermediate layer grows distally as new proximal micro-layers form. The outer layer is dragged distally by the intermediate layer as a result of its distal growth, for the three layers are closely packed to each other at their boundaries. Furthermore, the occurrence of the intermediate and inner layers in the distal portion of the rostral bone may be because the distal end of the beak is frequently used and worn, and the rhinotheca therefore needs to be replaced more frequently at the distal end. The rhinotheca structure described here will be an important and useful factor in the reconstruction of the beaks of birds in extinct taxa.

How does the curvature of the upper beak bone reflect the overlying rhinotheca morphology?

The beak has independently been evolved accompanied by the edentulism in many tetrapod linages, including extant Testudinata and Aves, and its form and function have been greatly diversified. The beak is formed by beak bones and the overlying keratinous cover, although their profiles are different from each other. Therefore, it is difficult to reliably reconstruct the entire profile of the beak in extinct taxa, whose keratinous tissues are rarely preserved. For elucidation of the morphological relationship between beak bone and overlying keratinous cover, we compared the curvature distribution of the culminal profiles of the upper beak bone and the overlying keratinous cover (rhinotheca) with each other using CT-scan, in 66 extant testudinatan and avian specimens (Aves: 33 genera, 24 families; Testudinata: 12 genera seven families). In both, rhinotheca and beak bone, the curvature of the profile was nearly constant rostral to a certain point, which was defined as the transition point, and the transition points of the rhinotheca and beak bone were close to each other. The profiles of the rhinotheca and beak bone rostral to their transition point were different in curvature and length. However, the ratio between the curvatures of rhinotheca and the beak bone strongly correlated with the arc angle of the rostral culminal profiles of the beak bone. The upper beak profile in extinct taxa is expected to be reconstructed more reliably using the abovementioned relationship between the beak bone and the rhinotheca.

Early neonatal loss of inhibitory synaptic input to the spinal motor neurons confers spina bifida-like leg dysfunction in a chicken model.

Spina bifida aperta (SBA), one of the most common congenital malformations, causes lifelong neurological complications, particularly in terms of motor dysfunction. Fetuses with SBA exhibit voluntary leg movements in utero and during early neonatal life, but these disappear within the first few weeks after birth. However, the pathophysiological sequence underlying such motor dysfunction remains unclear. Additionally, because important insights have yet to be obtained from human cases, an appropriate animal model is essential. Here, we investigated the neuropathological mechanisms of progression of SBA-like motor dysfunctions in a neural tube surgery-induced chicken model of SBA at different pathogenesis points ranging from embryonic to posthatch ages. We found that chicks with SBA-like features lose voluntary leg movements and subsequently exhibit lower-limb paralysis within the first 2 weeks after hatching, coinciding with the synaptic change-induced disruption of spinal motor networks at the site of the SBA lesion in the lumbosacral region. Such synaptic changes reduced the ratio of inhibitory-to-excitatory inputs to motor neurons and were associated with a drastic loss of γ-aminobutyric acid (GABA)ergic inputs and upregulation of the cholinergic activities of motor neurons. Furthermore, most of the neurons in ventral horns, which appeared to be suffering from excitotoxicity during the early postnatal days, underwent apoptosis. However, the triggers of cellular abnormalization and neurodegenerative signaling were evident in the middle- to late-gestational stages, probably attributable to the amniotic fluid-induced in ovo milieu. In conclusion, we found that early neonatal loss of neurons in the ventral horn of exposed spinal cord affords novel insights into the pathophysiology of SBA-like leg dysfunction.

Morphological variation in brain through domestication of fowl.

Great variations in the size, shape, color, feather structure and behavior are observed among fowl breeds. Because many types of domestic fowls have been bred for various purposes, they are ideal to assess the relationship between brain morphology and avian biology. However, little is known about changes in brain shape that may have occurred during fowl domestication. We analyzed the brains of red jungle fowl and domestic fowl to clarify differences in the brain shape between these breeds, as well as the shape changes associated with size enlargement using three-dimensional geometric morphometrics. Principal component and multivariate regression analyses showed that ventrodorsal bending, anteroposterior elongation and width reduction were significantly correlated with brain size. According to the size-dependent analysis, the red jungle fowl brain has an intermediate shape between the brain of young broilers and that of large domestic fowl and adult broilers. After the size effect is removed, geometric morphometric analyses show that the brain of red jungle fowl is different from that of domestic fowl, with large round cerebral hemispheres. Significant correlations exist between the skull length and brain volume among fowl, while the brain volume relative to the skull length is distinctly larger in red jungle fowl compared with domestic fowl. The distinct brain shape and increased relative brain size of red jungle fowl may be driven by the presence of large, rounded cerebral hemispheres.

Interneurons secrete prosaposin, a neurotrophic factor, to attenuate kainic acid-induced neurotoxicity.

Prosaposin (PS) is a secretory neurotrophic factor, as well as a regulator of lysosomal enzymes. We previously reported the up-regulation of PS and the possibility of its axonal transport by GABAergic interneurons after exocitotoxicity induced by kainic acid (KA), a glutamate analog. In the present study, we performed double immunostaining with PS and three calcium binding protein markers: parvalbumin (PV), calbindin, and calretinin, for the subpopulation of GABAergic interneurons, and clarified that the increased PS around the hippocampal pyramidal neurons after KA injection existed mainly in the axons of PV positive interneurons. Electron microscopy revealed PS containing vesicles in the PV positive axon. Double immunostaining with PS and secretogranin or synapsin suggested that PS is secreted with secretogranin from synapses. Based on the results from in situ hybridization with two alternative splicing forms of PS mRNA, the increase of PS in the interneurons was due to the increase of PS + 0 (mRNA without 9-base insertion) as in the choroid plexus, but not PS + 9 (mRNA with 9-base insertion). These results were similar to those from the choroid plexus, which secretes an intact form PS + 0 to the cerebrospinal fluid. Neurons, especially PV positive GABAergic interneurons, produce and secrete the intact form of PS around hippocampal pyramidal neurons to protect them against KA neurotoxicity.

Studying avian encephalization with geometric morphometrics.

Encephalization is a core concept in comparative neurobiology, aiming to quantify the neurological capacity of organisms. For measuring encephalization, many studies have employed relative brain sizes corrected for expected allometric scaling to body size. Here we highlight the utility of a multivariate geometric morphometric (GM) approach for visualizing and analyzing neuroanatomical shape variation associated with encephalization. GM readily allows the statistical evaluation of covariates, such as size, and many software tools exist for visualizing their effects on shape. Thus far, however, studies using GM have not attempted to translate the meaning of encephalization to shape data. As such, we tested the statistical relationship between size and encephalization quotients (EQs) to brain shape utilizing a broad interspecific sample of avian endocranial data. Although statistically significant, the analyses indicate that allometry accounts for <10% of total neuroanatomical shape variation. Notably, we find that EQs, despite being corrected for allometric scaling based on size, contain size-related neuroanatomical shape changes. In addition, much of what is traditionally considered encephalization comprises clade-specific trends in relative forebrain expansion, particularly driven by landbirds. EQs, therefore, fail to capture 90% of the total neuroanatomical variation after correcting for allometry and shared phylogenetic history. Moving forward, GM techniques provide crucial tools for investigating key drivers of this vast, largely unexplored aspect of avian brain morphology.

A bizarre theropod from the Early Cretaceous of Japan highlighting mosaic evolution among coelurosaurians.

Our understanding of coelurosaurian evolution, particularly of bird origins, has been greatly improved, mainly due to numerous recently discovered fossils worldwide. Nearly all these discoveries are referable to the previously known coelurosaurian subgroups. Here, we report a new theropod, Fukuivenator paradoxus, gen. et sp. nov., based on a nearly complete specimen from the Lower Cretaceous Kitadani Formation of the Tetori Group, Fukui, Japan. While Fukuivenator possesses a large number of morphological features unknown in any other theropod, it has a combination of primitive and derived features seen in different theropod subgroups, notably dromaeosaurid dinosaurs. Computed-tomography data indicate that Fukuivenator possesses inner ears whose morphology is intermediate between those of birds and non-avian dinosaurs. Our phylogenetic analysis recovers Fukuivenator as a basally branching maniraptoran theropod, yet is unable to refer it to any known coelurosaurian subgroups. The discovery of Fukuivenator considerably increases the morphological disparity of coelurosaurian dinosaurs and highlights the high levels of homoplasy in coelurosaurian evolution.

Correction: Ontogenetic Shape Change in the Chicken Brain: Implications for Paleontology.

[This corrects the article DOI: 10.1371/journal.pone.0129939.].

Ontogenetic Shape Change in the Chicken Brain: Implications for Paleontology.

Paleontologists have investigated brain morphology of extinct birds with little information on post-hatching changes in avian brain morphology. Without the knowledge of ontogenesis, assessing brain morphology in fossil taxa could lead to misinterpretation of the phylogeny or neurosensory development of extinct species. Hence, it is imperative to determine how avian brain morphology changes during post-hatching growth. In this study, chicken brain shape was compared at various developmental stages using three-dimensional (3D) geometric morphometric analysis and the growth rate of brain regions was evaluated to explore post-hatching morphological changes. Microscopic MRI (µMRI) was used to acquire in vivo data from living and post-mortem chicken brains. The telencephalon rotates caudoventrally during growth. This change in shape leads to a relative caudodorsal rotation of the cerebellum and myelencephalon. In addition, all brain regions elongate rostrocaudally and this leads to a more slender brain shape. The growth rates of each brain region were constant and the slopes from the growth formula were parallel. The dominant pattern of ontogenetic shape change corresponded with interspecific shape changes due to increasing brain size. That is, the interspecific and ontogenetic changes in brain shape due to increased size have similar patterns. Although the shape of the brain and each brain region changed considerably, the volume ratio of each brain region did not change. This suggests that the brain can change its shape after completing functional differentiation of the brain regions. Moreover, these results show that consideration of ontogenetic changes in brain shape is necessary for an accurate assessment of brain morphology in paleontological studies.

Variation in avian brain shape: relationship with size and orbital shape.

There is wide variation in brain shape among birds. Differences in brain dimensions reflect species-specific sensory capacities and behavioral repertoires that are shaped by environmental and biological factors during evolution. Most previous studies aimed at defining factors impacting brain shape have used volumetric or linear measurements. However, few have explored the quantitative indices of three-dimensional (3D) brain geometry that are absolutely imperative to understanding avian evolutionary history. This study aimed: (i) to explore the relationship between brain shape and overall brain size; and (ii) to assess the relationship between brain shape and orbital shape. Avian brain endocasts were reconstructed from computed tomography images and analyzed using 3D geometric morphometrics. Principal component analysis revealed dominant regional variations in avian brain shape and shape correlations between the telencephalon and cerebellum, between the cerebellum and myelencephalon, and between the diencephalon and optic tectum. Brain shape changes relative to total brain size were determined by multivariate regression analysis. Larger brain size was associated with a relatively slender telencephalon and differences in brain orientation. The correlation between brain shape and orbital shape was assessed by two-block partial least-squares analysis. Relatively round brains with a ventrally flexed brain base were associated with rounder orbits, while narrower brains with a flat brain base were associated with more elongated orbits. The shapes of functionally associated avian brain regions are correlated, and orbital size and shape are dominant factors influencing the overall shape of the avian brain.