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1.  Developmental basis for telencephalon expansion in waterfowl: enlargement prior to neurogenesis 
Some altricial and some precocial species of birds have evolved enlarged telencephalons compared with other birds. Previous work has shown that finches and parakeets, two species that hatch in an immature (i.e. altricial) state, enlarged their telencephalon by delaying telencephalic neurogenesis. To determine whether species that hatch in a relatively mature (i.e. precocial) state also enlarged their telencephalon by delaying telencephalic neurogenesis, we examined brain development in geese, ducks, turkeys and chickens, which are all precocial. Whereas the telencephalon occupies less than 55 per cent of the brain in chickens and turkeys, it occupies more than 65 per cent in ducks and geese. To determine how these species differences in adult brain region proportions arise during development, we examined brain maturation (i.e. neurogenesis timing) and estimated telencephalon, tectum and medulla volumes from serial Nissl-stained sections in the four species. We found that incubation time predicts the timing of neurogenesis in all major brain regions and that the telencephalon is proportionally larger in ducks and geese before telencephalic neurogenesis begins. These findings demonstrate that the expansion of the telencephalon in ducks and geese is achieved by altering development prior to neurogenesis onset. Thus, precocial and altricial species evolved different developmental strategies to expand their telencephalon.
doi:10.1098/rspb.2009.0888
PMCID: PMC2817193  PMID: 19605398
neurogenesis; Anseriformes; size; telencephalon; precocial; altricial
2.  Anatomical Specializations for Nocturnality in a Critically Endangered Parrot, the Kakapo (Strigops habroptilus) 
PLoS ONE  2011;6(8):e22945.
The shift from a diurnal to nocturnal lifestyle in vertebrates is generally associated with either enhanced visual sensitivity or a decreased reliance on vision. Within birds, most studies have focused on differences in the visual system across all birds with respect to nocturnality-diurnality. The critically endangered Kakapo (Strigops habroptilus), a parrot endemic to New Zealand, is an example of a species that has evolved a nocturnal lifestyle in an otherwise diurnal lineage, but nothing is known about its' visual system. Here, we provide a detailed morphological analysis of the orbits, brain, eye, and retina of the Kakapo and comparisons with other birds. Morphometric analyses revealed that the Kakapo's orbits are significantly more convergent than other parrots, suggesting an increased binocular overlap in the visual field. The Kakapo exhibits an eye shape that is consistent with other nocturnal birds, including owls and nightjars, but is also within the range of the diurnal parrots. With respect to the brain, the Kakapo has a significantly smaller optic nerve and tectofugal visual pathway. Specifically, the optic tectum, nucleus rotundus and entopallium were significantly reduced in relative size compared to other parrots. There was no apparent reduction to the thalamofugal visual pathway. Finally, the retinal morphology of the Kakapo is similar to that of both diurnal and nocturnal birds, suggesting a retina that is specialised for a crepuscular niche. Overall, this suggests that the Kakapo has enhanced light sensitivity, poor visual acuity and a larger binocular field than other parrots. We conclude that the Kakapo possesses a visual system unlike that of either strictly nocturnal or diurnal birds and therefore does not adhere to the traditional view of the evolution of nocturnality in birds.
doi:10.1371/journal.pone.0022945
PMCID: PMC3157909  PMID: 21860663
3.  Assessing Phylogenetic Relationships among Galliformes: A Multigene Phylogeny with Expanded Taxon Sampling in Phasianidae 
PLoS ONE  2013;8(5):e64312.
Galliform birds (relatives of the chicken and turkey) have attracted substantial attention due to their importance to society and value as model systems. This makes understanding the evolutionary history of Galliformes, especially the species-rich family Phasianidae, particularly interesting and important for comparative studies in this group. Previous studies have differed in their conclusions regarding galliform phylogeny. Some of these studies have suggested that specific clades within this order underwent rapid radiations, potentially leading to the observed difficulty in resolving their phylogenetic relationships. Here we presented analyses of six nuclear intron sequences and two mitochondrial regions, an amount of sequence data larger than many previous studies, and expanded taxon sampling by collecting data from 88 galliform species and four anseriform outgroups. Our results corroborated recent studies describing relationships among the major families, and provided further evidence that the traditional division of the largest family, the Phasianidae into two major groups (“pheasants” and “partridges”) is not valid. Within the Phasianidae, relationships among many genera have varied among studies and there has been little consensus for the placement of many taxa. Using this large dataset, with substantial sampling within the Phasianidae, we obtained strong bootstrap support to confirm some previously hypothesized relationships and we were able to exclude others. In addition, we added the first nuclear sequence data for the partridge and quail genera Ammoperdix, Caloperdix, Excalfactoria, and Margaroperdix, placing these taxa in the galliform tree of life with confidence. Despite the novel insights obtained by combining increased sampling of taxa and loci, our results suggest that additional data collection will be necessary to solve the remaining uncertainties.
doi:10.1371/journal.pone.0064312
PMCID: PMC3669371  PMID: 23741315
4.  Extrinsic Embryonic Sensory Stimulation Alters Multimodal Behavior and Cellular Activation 
Developmental neurobiology  2008;68(13):1463-1473.
Embryonic vision is generated and maintained by spontaneous neuronal activation patterns, yet extrinsic stimulation also sculpts sensory development. Because the sensory and motor systems are interconnected in embryogenesis, how extrinsic sensory activation guides multimodal differentiation is an important topic. Further, it is unknown whether extrinsic stimulation experienced near sensory sensitivity onset contributes to persistent brain changes, ultimately affecting postnatal behavior. To determine the effects of extrinsic stimulation on multimodal development, we delivered auditory stimulation to bobwhite quail groups during early, middle, or late embryogenesis, and then tested postnatal behavioral responsiveness to auditory or visual cues. Auditory preference tendencies were more consistently toward the conspecific stimulus for animals stimulated during late embryogenesis. Groups stimulated during middle or late embryogenesis showed altered postnatal species-typical visual responsiveness, demonstrating a persistent multimodal effect. We also examined whether auditory-related brain regions are receptive to extrinsic input during middle embryogenesis by measuring postnatal cellular activation. Stimulated birds showed a greater number of ZENK-immunopositive cells per unit volume of brain tissue in deep optic tectum, a midbrain region strongly implicated in multimodal function. We observed similar results in the medial and caudomedial nidopallia in the telencephalon. There were no ZENK differences between groups in inferior colliculus or in caudolateral nidopallium, avian analog to prefrontal cortex. To our knowledge, these are the first results linking extrinsic stimulation delivered so early in embryogenesis to changes in postnatal multimodal behavior and cellular activation. The potential role of competitive interactions between the sensory and motor systems is discussed.
doi:10.1002/dneu.20667
PMCID: PMC2647013  PMID: 18777564
embryogenesis; extrinsic stimulation; multimodal behavior; midbrain; cellular activation
5.  Distribution of an endogenous lectin in the developing chick optic tectum 
The Journal of Cell Biology  1978;79(2):491-499.
We determined the cellular localization of an endogenous lectin at various times during the development of a well-characterized region of chick brain, the optic tectum. This lectin is a carbohydrate-binding protein that interacts with lactose and other saccharides, undergoes striking changes in specific activity with development, and has previously been purified by affinity chromatography from extracts of embryonic chick brain and muscle. Cellular localization in the tectum was done by indirect immunofluoresecent staining, using immunoglobulin G derived from an antiserum raised against pure lectin. No lectin was detectable in the optic tectum examined at 5 days of embryonic development. From approximately 7 days of development, neuronal cell bodies and fibers were labeled by the antibody; and extracts of tectum contained hemagglutination activity that could be inhibited by lactose or by the antiserum. Lectin remained present in many tectal neuronal layers after hatching; but in 2-month-old chicks it was sparse or absent in most of the tectum except for prominent labeling of fibers in the stratum album centrale. The initial appearance of lectin in the optic tectum was not dependent on innervation by optic nerve fibers since bilateral enucleation during embryogenesis did not affect it. Lectin was detectable on the surface of embryonic optic tectal neurons dissociated with a buffer containing EDTA.
PMCID: PMC2110234  PMID: 721897
6.  Distribution and Development of Nicotinic Acetylcholine Receptor Subtypes in the Optic Tectum of Rana pipiens 
Acetylcholine allows the elicitation of visually evoked behaviors mediated by the frog optic tectum, but the mechanisms behind its effects are unknown. Although nicotinic acetylcholine receptors (nAChRs) exist in the tectum, their subtype has not been assessed. By using quantitative autoradiography, we examined the binding of [3H]cytisine and [125I]α-bungarotoxin in the laminated tectum. In mammalian systems, these radioligands bind with high affinity to α4 nAChR subunits and α7 nAChR subunits, respectively. [3H]Cytisine demonstrated high specific binding in adult frogs in retinorecipient layer 9, intermediate densities in layer 8, and low binding in layers 1–7 of the tectum. [3H]Cytisine binding was significantly higher in the tecta of adults than in those of tadpoles. Lesioning the optic nerve for 6 weeks decreased [3H]cytisine binding in layers 8/9 by 70 ± 1%, whereas 6-month lesions decreased binding by 76 ± 3%. Specific binding of [125I]α-bungarotoxin in adults was present only at intermediate levels in tectal layers 8 and 9, and undetectable in the deeper tectal layers. However, the nucleus isthmi, a midbrain structure reciprocally connected to the tectum, exhibited high levels of binding. There were no significant differences in tectal [125I]α-bungarotoxin binding between tadpoles and adults. Six-week lesions of the optic nerve decreased tectal [125I]α-bungarotoxin binding by 33 ± 10%, but 6-month lesions had no effect. The pharmacokinetic characteristics of [3H]cytisine and [125I]α-bungarotoxin binding in the frog brain were similar to those demonstrated in several mammalian species. These results indicate that [3H]cytisine and [125I]α-bungarotoxin identify distinct nAChR subtypes in the tectum that likely contain non-α7 and α7 subunits, respectively. The majority of non-α7 receptors are likely associated with retinal ganglion cell terminals, whereas α7-containing receptors appear to have a different localization.
PMCID: PMC2265082  PMID: 10880991
cholinergic; visual system; autoradiography
7.  Sequencing of the core MHC region of black grouse (Tetrao tetrix) and comparative genomics of the galliform MHC 
BMC Genomics  2012;13:553.
Background
The MHC, which is regarded as the most polymorphic region in the genomes of jawed vertebrates, plays a central role in the immune system by encoding various proteins involved in the immune response. The chicken MHC-B genomic region has a highly streamlined gene content compared to mammalian MHCs. Its core region includes genes encoding Class I and Class IIB molecules but is only ~92Kb in length. Sequences of other galliform MHCs show varying degrees of similarity as that of chicken. The black grouse (Tetrao tetrix) is a wild galliform bird species which is an important model in conservation genetics and ecology. We sequenced the black grouse core MHC-B region and combined this with available data from related species (chicken, turkey, gold pheasant and quail) to perform a comparative genomics study of the galliform MHC. This kind of analysis has previously been severely hampered by the lack of genomic information on avian MHC regions, and the galliformes is still the only bird lineage where such a comparison is possible.
Results
In this study, we present the complete genomic sequence of the MHC-B locus of black grouse, which is 88,390 bp long and contains 19 genes. It shows the same simplicity as, and almost perfect synteny with, the corresponding genomic region of chicken. We also use 454-transcriptome sequencing to verify expression in 17 of the black grouse MHC-B genes. Multiple sequence inversions of the TAPBP gene and TAP1-TAP2 gene block identify the recombination breakpoints near the BF and BLB genes. Some of the genes in the galliform MHC-B region also seem to have been affected by selective forces, as inferred from deviating phylogenetic signals and elevated rates of non-synonymous nucleotide substitutions.
Conclusions
We conclude that there is large synteny between the MHC-B region of the black grouse and that of other galliform birds, but that some duplications and rearrangements have occurred within this lineage. The MHC-B sequence reported here will provide a valuable resource for future studies on the evolution of the avian MHC genes and on links between immunogenetics and ecology of black grouse.
doi:10.1186/1471-2164-13-553
PMCID: PMC3500228  PMID: 23066932
8.  Retinotopic order in the absence of axon competition 
Nature  2008;452(7189):892-895.
The retinotectal projection has long been studied experimentally and theoretically, as a model for the formation of topographic brain maps1-3. Neighbouring retinal ganglion cells (RGCs) project their axons to neighbouring positions in the optic tectum, thus reestablishing a continuous neural representation of visual space. Mapping along this axis requires chemorepellent signalling from tectal cells, expressing ephrin-A ligands, to retinal growth cones, expressing EphA receptors4. High concentrations of ephrin A, increasing from anterior to posterior, prevent temporal axons from invading the posterior tectum. However, the force that drives nasal axons to extend past the anterior tectum and terminate in posterior regions remains to be identified. We tested whether axon–axon interactions, such as competition, are required for posterior tectum innervation. By transplanting blastomeres from a wild-type (WT) zebrafish into a lakritz (lak) mutant, which lacks all RGCs5, we created chimaeras with eyes that contained single RGCs. These solitary RGCs often extended axons into the tectum, where they branched to form a terminal arbor. Here we show that the distal tips of these arbors were positioned at retinotopically appropriate positions, ruling out an essential role for competition in innervation of the ephrin-A-rich posterior tectum. However, solitary arbors were larger and more complex than under normal, crowded conditions, owing to a lack of pruning of proximal branches during refinement of the retinotectal projection. We conclude that dense innervation is not required for targeting of retinal axons within the zebrafish tectum but serves to restrict arbor size and shape.
doi:10.1038/nature06816
PMCID: PMC2885002  PMID: 18368050
9.  Expression patterns of Ephs and ephrins throughout retinotectal development in Xenopus laevis 
Developmental neurobiology  2012;72(4):547-563.
The Eph family of receptor tyrosine kinases and their ligands the ephrins play an essential role in the targeting of retinal ganglion cell axons to topographically correct locations in the optic tectum during visual system development. The African claw-toed frog Xenopus laevis is a popular animal model for the study of retinotectal development because of its amenability to live imaging and electrophysiology. Its visual system undergoes protracted growth continuing beyond metamorphosis, yet little is known about ephrin and Eph expression patterns beyond stage 39 when retinal axons first arrive in the tectum. We used alkaline phosphatase fusion proteins of EphA3, ephrin-A5, EphB2, and ephrin-B1 as affinity probes to reveal the expression patterns of ephrin-As, EphAs, ephrin-Bs and EphBs, respectively. Analysis of brains from stage 39 to adult frog revealed that ephrins and Eph receptors are expressed throughout development. As observed in other species, staining for ephrin-As displayed a high caudal to low rostral expression pattern across the tectum, roughly complementary to the expression of EphAs. In contrast with the current model, EphBs were found to be expressed in the tectum in a high dorsal to low ventral gradient in young animals. In animals with induced binocular tectal innervation, ocular dominance bands of alternating input from the two eyes formed in the tectum; however, ephrin-A and EphA expression patterns were unmodulated and similar to those in normal frogs, confirming that the segregation of axons into eye-specific stripes is not the consequence of a respecification of molecular guidance cues in the tectum.
doi:10.1002/dneu.20930
PMCID: PMC3395774  PMID: 21656698
visual system; axon guidance; topographic mapping; optic tectum; ocular dominance
10.  FGF2 Delays Tectal Neurogenesis, Increases Tectal Cell Numbers, and Alters Tectal Lamination in Embryonic Chicks 
PLoS ONE  2013;8(11):e79949.
Intraventricular injections of the fibroblast growth factor 2 (FGF2) are known to increase the size of the optic tectum in embryonic chicks. Here we show that this increase in tectum size is due to a delay in tectal neurogenesis, which by definition extends the proliferation of tectal progenitors. Specifically, we use cumulative labeling with the thymidine analog EdU to demonstrate that FGF2 treatment on embryonic day 4 (ED4) reduces the proportion and absolute number of unlabeled cells in the rostroventral tectum when EdU infusions are begun on ED5, as one would expect if FGF2 retards tectal neurogenesis. We also examined FGF2′s effect on neurogenesis in the caudodorsal tectum, which is born 2-3 days after the rostroventral tectum, by combining FGF2 treatment on ED4 with EDU infusions beginning on ED8. Again, FGF2 treatment reduced the proportion and number of EdU-negative (i.e., unlabeled) cells, consistent with a delay in neurogenesis. Collectively, these data indicate FGF2 in embryonic chicks delays neurogenesis throughout much of the tectum and continues to do so for several days after the FGF2 injection. One effect of this delay in neurogenesis is that tectal cell numbers more than double. In addition, tectal laminae that are born early in development become abnormally thin and cell-sparse after FGF2 treatment, whereas late-born layers remain unaffected. Combined with the results of prior work, these data indicate that FGF2 delays tectal neurogenesis and, thereby, triggers a cascade of changes in tectum size and morphology.
doi:10.1371/journal.pone.0079949
PMCID: PMC3827156  PMID: 24265789
11.  A mitogenomic perspective on the ancient, rapid radiation in the Galliformes with an emphasis on the Phasianidae 
Background
The Galliformes is a well-known and widely distributed Order in Aves. The phylogenetic relationships of galliform birds, especially the turkeys, grouse, chickens, quails, and pheasants, have been studied intensively, likely because of their close association with humans. Despite extensive studies, convergent morphological evolution and rapid radiation have resulted in conflicting hypotheses of phylogenetic relationships. Many internal nodes have remained ambiguous.
Results
We analyzed the complete mitochondrial (mt) genomes from 34 galliform species, including 14 new mt genomes and 20 published mt genomes, and obtained a single, robust tree. Most of the internal branches were relatively short and the terminal branches long suggesting an ancient, rapid radiation. The Megapodiidae formed the sister group to all other galliforms, followed in sequence by the Cracidae, Odontophoridae and Numididae. The remaining clade included the Phasianidae, Tetraonidae and Meleagrididae. The genus Arborophila was the sister group of the remaining taxa followed by Polyplectron. This was followed by two major clades: ((((Gallus, Bambusicola) Francolinus) (Coturnix, Alectoris)) Pavo) and (((((((Chrysolophus, Phasianus) Lophura) Syrmaticus) Perdix) Pucrasia) (Meleagris, Bonasa)) ((Lophophorus, Tetraophasis) Tragopan))).
Conclusions
The traditional hypothesis of monophyletic lineages of pheasants, partridges, peafowls and tragopans was not supported in this study. Mitogenomic analyses recovered robust phylogenetic relationships and suggested that the Galliformes formed a model group for the study of morphological and behavioral evolution.
doi:10.1186/1471-2148-10-132
PMCID: PMC2880301  PMID: 20444289
12.  Regulation of the development of tectal neurons and their projections by transcription factors Brn3a and Pax7 
Developmental biology  2008;316(1):6-20.
The rostral part of the dorsal midbrain, known as the superior colliculus in mammals or the optic tectum in birds, receives a substantial retinal input and plays a diverse and important role in sensorimotor integration. However, little is known about the development of specific subtypes of neurons in the tectum, particularly those which contribute tectofugal projections to the thalamus, isthmic region, and hindbrain. Here we show that two homeodomain transcription factors, Brn3a and Pax7, are expressed in mutually exclusive patterns in the developing and mature avian midbrain. Neurons expressing these factors are generated at characteristic developmental times, and have specific laminar fates within the tectum. In mice expressing βgalactosidase targeted to the Pou4f1 (Brn3a) locus, Brn3a-expressing neurons contribute to the ipsilateral but not the contralateral tectofugal projections to the hindbrain. Using misexpression of Brn3a and Pax7 by electroporation in the chick tectum, combined with GFP reporters, we show that Brn3a determines the laminar fate of subsets of tectal neurons. Furthermore, Brn3a regulates the development of neurons contributing to specific ascending and descending tectofugal pathways, while Pax7 globally represses the development of tectofugal projections to nearly all brain structures.
doi:10.1016/j.ydbio.2007.12.040
PMCID: PMC2396191  PMID: 18280463
Brn3; Brn3a; Pou4f1; POU-domain; Pax7; superior colliculus; midbrain; tectofugal; tectospinal; tectobulbar
13.  Mapping of the Receptive Fields in the Optic Tectum of Chicken (Gallus gallus) Using Sparse Noise 
PLoS ONE  2013;8(4):e60782.
The optic tectum plays a key role in visual processing in birds. While the input from the retina is topographic in the superficial layers, the deep layers project to the thalamic nucleus rotundus in a functional topographical manner. Although the receptive fields of tectal neurons in birds have been mapped before, a high resolution description of the white and black subfields of the receptive fields of tectal neurons is not available. We measured the receptive fields of neurons in the different layers of the tectum of anesthetized chickens with black and white stimuli that were flashed on a grey background in fast progression. Our results show that neurons in the deep layers of the optic tectum tend to respond stronger to black stimuli compared to white stimuli. In addition, the receptive field sizes are larger when measured using black stimuli than with white stimuli. While the black subfield was significantly larger than the white subfield for the intermediate and deep layers, no significant effects were found for the superficial layers. Finally, we investigated the optimal stimulus size in a subset of the neurons and found that these cells respond best to small white stimuli and to large black stimuli. In the majority of the cases the response was stronger to a large black bar than to a small white bar. We propose that such a stronger response to black stimuli might be advantageous for the detection of darker objects against the brighter sky.
doi:10.1371/journal.pone.0060782
PMCID: PMC3620443  PMID: 23593310
14.  Developmental Modes and Developmental Mechanisms can Channel Brain Evolution 
Anseriform birds (ducks and geese) as well as parrots and songbirds have evolved a disproportionately enlarged telencephalon compared with many other birds. However, parrots and songbirds differ from anseriform birds in their mode of development. Whereas ducks and geese are precocial (e.g., hatchlings feed on their own), parrots and songbirds are altricial (e.g., hatchlings are fed by their parents). We here consider how developmental modes may limit and facilitate specific changes in the mechanisms of brain development. We suggest that altriciality facilitates the evolution of telencephalic expansion by delaying telencephalic neurogenesis. We further hypothesize that delays in telencephalic neurogenesis generate delays in telencephalic maturation, which in turn foster neural adaptations that facilitate learning. Specifically, we propose that delaying telencephalic neurogenesis was a prerequisite for the evolution of neural circuits that allow parrots and songbirds to produce learned vocalizations. Overall, we argue that developmental modes have influenced how some lineages of birds increased the size of their telencephalon and that this, in turn, has influenced subsequent changes in brain circuits and behavior.
doi:10.3389/fnana.2011.00004
PMCID: PMC3037498  PMID: 21369349
bird; mode; development; proliferation; evolution
15.  Post-Proliferative Immature Radial Glial Cells Female-Specifically Express Aromatase in the Medaka Optic Tectum 
PLoS ONE  2013;8(9):e73663.
Aromatase, the key enzyme responsible for estrogen biosynthesis, is present in the brain of all vertebrates. Much evidence has accumulated that aromatase is highly and exclusively expressed in proliferating mature radial glial cells in the brain of teleost fish even in adulthood, unlike in other vertebrates. However, the physiological significance of this expression remains unknown. We recently found that aromatase is female-specifically expressed in the optic tectum of adult medaka fish. In the present study, we demonstrated that, contrary to the accepted view of the teleost brain, female-specific aromatase-expressing cells in the medaka optic tectum represent a transient subset of post-proliferative immature radial glial cells in the neural stem cell lineage. This finding led us to hypothesize that female-specific aromatase expression and consequent estrogen production causes some sex difference in the life cycle of tectal cells. As expected, the female tectum exhibited higher expression of genes indicative of cell proliferation and radial glial maturation and lower expression of an anti-apoptotic gene than did the male tectum, suggesting a female-biased acceleration of the cell life cycle. Complicating the interpretation of this result, however, is the additional observation that estrogen administration masculinized the expression of these genes in the optic tectum, while simultaneously stimulating aromatase expression. Taken together, these results provide evidence that a unique subpopulation of neural stem cells female-specifically express aromatase in the optic tectum and suggest that this aromatase expression and resultant estrogen synthesis have an impact on the life cycle of tectal cells, whether stimulatory or inhibitory.
doi:10.1371/journal.pone.0073663
PMCID: PMC3760802  PMID: 24019933
16.  EphA3 Expressed in the Chicken Tectum Stimulates Nasal Retinal Ganglion Cell Axon Growth and Is Required for Retinotectal Topographic Map Formation 
PLoS ONE  2012;7(6):e38566.
Background
Retinotopic projection onto the tectum/colliculus constitutes the most studied model of topographic mapping and Eph receptors and their ligands, the ephrins, are the best characterized molecular system involved in this process. Ephrin-As, expressed in an increasing rostro-caudal gradient in the tectum/colliculus, repel temporal retinal ganglion cell (RGC) axons from the caudal tectum and inhibit their branching posterior to their termination zones. However, there are conflicting data regarding the nature of the second force that guides nasal axons to invade and branch only in the caudal tectum/colliculus. The predominant model postulates that this second force is produced by a decreasing rostro-caudal gradient of EphA7 which repels nasal optic fibers and prevents their branching in the rostral tectum/colliculus. However, as optic fibers invade the tectum/colliculus growing throughout this gradient, this model cannot explain how the axons grow throughout this repellent molecule.
Methodology/Principal Findings
By using chicken retinal cultures we showed that EphA3 ectodomain stimulates nasal RGC axon growth in a concentration dependent way. Moreover, we showed that nasal axons choose growing on EphA3-expressing cells and that EphA3 diminishes the density of interstitial filopodia in nasal RGC axons. Accordingly, in vivo EphA3 ectodomain misexpression directs nasal optic fibers toward the caudal tectum preventing their branching in the rostral tectum.
Conclusions
We demonstrated in vitro and in vivo that EphA3 ectodomain (which is expressed in a decreasing rostro-caudal gradient in the tectum) is necessary for topographic mapping by stimulating the nasal axon growth toward the caudal tectum and inhibiting their branching in the rostral tectum. Furthermore, the ability of EphA3 of stimulating axon growth allows understanding how optic fibers invade the tectum growing throughout this molecular gradient. Therefore, opposing tectal gradients of repellent ephrin-As and of axon growth stimulating EphA3 complement each other to map optic fibers along the rostro-caudal tectal axis.
doi:10.1371/journal.pone.0038566
PMCID: PMC3369860  PMID: 22685584
17.  Pharmacology, Distribution and Development of Muscarinic Acetylcholine Receptor Subtypes in the Optic Tectum of Rana Pipiens 
Neuroscience  2001;104(1):161-179.
Visually evoked behaviors mediated by the frog optic tectum require cholinergic activity, but the receptor subtypes through which acetylcholine acts are not yet identified. Using quantitative autoradiography and scintillation spectrometry, we examined the binding of [3H]pirenzepine and [3H]AF-DX 384 in the laminated optic tectum of the frog. In mammalian systems, these substances bind excitatory (m1 and m3 subtypes) and inhibitory (m2 and m4 subtypes) muscarinic acetylcholine receptors, respectively. Pharmacological analyses, including the use of specific muscarinic toxins, confirmed the subtype selectivity of the radioligands in the frog brain. Binding sites for [3H]pirenzepine were distinct from those for [3H]AF-DX 384. In the adult tectum, [3H]pirenzepine demonstrated specific binding in tectal layers 5–9. [3H]Pirenzepine binding was also present in tadpoles as young as stage V, but all sampled stages of tadpole tectum had significantly less binding when compared to adults. Lesioning of the optic nerve had no effect on [3H]pirenzepine binding. Specific [3H]AF-DX 384 binding was found in all layers of the adult tectum. All sampled tadpole stages exhibited binding sites for [3H]AF-DX 384, but the densities of these sites were also significantly higher in adults than they were in developing stages. Short-term lesions of the optic nerve reduced [3H]AF-DX 384 binding in all tectal layers of the deafferented lobe when compared to the afferented one. Long-term lesions decreased [3H]AF-DX 384 sites in both lobes.
These results indicate that multiple muscarinic acetylcholine receptor binding sites reside in the frog optic tectum at all stages of development, and their pharmacology resembles that of mammalian m1/m3, m2 and m4 subtypes. Our data indicate that few, if any, of these receptors are likely to be located on retinal ganglion cell terminals. Furthermore, the expression of inhibitory muscarinic subtypes seems to be regulated by different mechanisms than that for excitatory subtypes.
PMCID: PMC2266691  PMID: 11311540
cholinergic; visual plasticity; autoradiography; amphibia
18.  The Natural Reservoirs of Salmonella Enteritidis in Populations of Wild Birds 
Objective
The aim of our study was to identify possible natural reservoirs of Salmonella Enteritidis among wild birds.
Introduction
Salmonella Enteritidis is dangerous for human due the reason of toxicoinfaction. These pathogen demonstrate high virulence for small children and people with chronic pathologies and can causes people die. The main source of infection to humans is birds (poultry and wild).
Wild birds represent the natural reservoir of same bacterial pathogens. It is known that Salmonella can occupy an intestinal tract of birds. This colonization in general is constant, sometimes proceeds with an alternating fever, and usually, without clinical signs. Infected birds can transmit pathogens to other isolates in close contact. This usually occurs on the nesting during seasonal migrations. In the southern region of Ukraine are several points of intersection of migration routes of wild birds on the way from Europe to Africa and Asia (National Park “Askania Nova”and others).
Methods
The study was conducted in populations of wild birds in National Park “Askania Nova” and peninsula “Arabat arrow” (the Azov Sea coast). From bird selected samples of blood serum and egg yolks for research in serum plate agglutination test (SPA) and litter samples for bacteriological research.
Results
The serological monitoring in populations of wild waterfowl in National Park “Askania Nova” (Ichthyaetus relictus, Sterna nilotica, Sterna herundo, Casarca ferruginea) has shown the presence of seropozitive individuals in adult birds (average 18%) and egg yolks (avarrage 12%). The bacteriological investigations confirmed circulation of Salmonella in this group of birds. 32.3% of all bacterial pathogens was Salmonella and more then half of them was the reprezentatives of serovar Salmonella Enteritidis.
Similar studies were conducted on territory of peninsula “Arabat arrow” (the Azov Sea coast). The serological monitoring among of wild waterfowl (Ardea cinerea, Sterna caspia, Phalacrocorax carbo, Podiceps cristatus, Anas platyrhynchos, Cygnus olar) revealed the presence of antibodies in blood serum (avarrage 17%) and egg yolks (avarrage 10%). From litter samples was isolated a great deal of Enterobacteria (Escherichia coli. Salmonella, Citrobacter, Enterobacter), havever 34.8% of them were Salmonella and near half of Salmonella (53.2%) was reprezentatives of serovar Salmonella Enteritidis.
Conclusions
It is proved that M. gallisepticum can persist among decorative waterfowl for her welfare with Galliformes, while waterfowl is a reservoir of the pathogen. Also natural reservoirs of Mycoplasma can be wild waterfowl (Casarca ferruginea). Such groups (populations) of birds may serve as a source of infection for commercial herds.
This shows that wild waterfowl are the natural reservoir for these dangerous pathogens like Salmonella Enteritidis. The carriers may account for 17–18% of all individuals in the population. In nesting different species of wild birds may be infected by Salmonella Enteritidis. In the process of migrating wild birds can carry Salmonella Enteritidis over long distances and is a threat to commercial poultry flocks and humans.
PMCID: PMC3692822
Salmonella Enteritidis; natural reservoir; wild birds
19.  Interspecies Avian Brain Chimeras Reveal That Large Brain Size Differences Are Influenced by Cell–Interdependent Processes 
PLoS ONE  2012;7(7):e42477.
Like humans, birds that exhibit vocal learning have relatively delayed telencephalon maturation, resulting in a disproportionately smaller brain prenatally but enlarged telencephalon in adulthood relative to vocal non-learning birds. To determine if this size difference results from evolutionary changes in cell-autonomous or cell-interdependent developmental processes, we transplanted telencephala from zebra finch donors (a vocal-learning species) into Japanese quail hosts (a vocal non-learning species) during the early neural tube stage (day 2 of incubation), and harvested the chimeras at later embryonic stages (between 9–12 days of incubation). The donor and host tissues fused well with each other, with known major fiber pathways connecting the zebra finch and quail parts of the brain. However, the overall sizes of chimeric finch telencephala were larger than non-transplanted finch telencephala at the same developmental stages, even though the proportional sizes of telencephalic subregions and fiber tracts were similar to normal finches. There were no significant changes in the size of chimeric quail host midbrains, even though they were innervated by the physically smaller zebra finch brain, including the smaller retinae of the finch eyes. Chimeric zebra finch telencephala had a decreased cell density relative to normal finches. However, cell nucleus size differences between each species were maintained as in normal birds. These results suggest that telencephalic size development is partially cell-interdependent, and that the mechanisms controlling the size of different brain regions may be functionally independent.
doi:10.1371/journal.pone.0042477
PMCID: PMC3408455  PMID: 22860132
20.  In Vivo Spike-Timing-Dependent Plasticity in the Optic Tectum of Xenopus Laevis 
Spike-timing-dependent plasticity (STDP) is found in vivo in a variety of systems and species, but the first demonstrations of in vivo STDP were carried out in the optic tectum of Xenopus laevis embryos. Since then, the optic tectum has served as an excellent experimental model for studying STDP in sensory systems, allowing researchers to probe the developmental consequences of this form of synaptic plasticity during early development. In this review, we will describe what is known about the role of STDP in shaping feed-forward and recurrent circuits in the optic tectum with a focus on the functional implications for vision. We will discuss both the similarities and differences between the optic tectum and mammalian sensory systems that are relevant to STDP. Finally, we will highlight the unique properties of the embryonic tectum that make it an important system for researchers who are interested in how STDP contributes to activity-dependent development of sensory computations.
doi:10.3389/fnsyn.2010.00007
PMCID: PMC3059697  PMID: 21423493
spike-timing-dependent plasticity; visual system; synaptic development; optic tectum; receptive field
21.  Direction selectivity in the visual system of the zebrafish larva 
Neural circuits in the vertebrate retina extract the direction of object motion from visual scenes and convey this information to sensory brain areas, including the optic tectum. It is unclear how computational layers beyond the retina process directional inputs. Recent developmental and functional studies in the zebrafish larva, using minimally invasive optical imaging techniques, indicate that direction selectivity might be a genetically hardwired property of the zebrafish brain. Axons from specific direction-selective (DS) retinal ganglion cells appear to converge on distinct laminae in the superficial tectal neuropil where they serve as inputs to DS postsynaptic neurons of matching specificity. In addition, inhibitory recurrent circuits in the tectum might strengthen the DS response of tectal output neurons. Here we review these recent findings and discuss some controversies with a particular focus on the zebrafish tectum’s role in extracting directional features from moving visual scenes.
doi:10.3389/fncir.2013.00111
PMCID: PMC3685220  PMID: 23785314
visual system; direction selectivity; zebrafish; optic tectum; neural circuits
22.  Perineuronal satellite neuroglia in the telencephalon of New Caledonian crows and other Passeriformes: evidence of satellite glial cells in the central nervous system of healthy birds? 
PeerJ  2013;1:e110.
Glia have been implicated in a variety of functions in the central nervous system, including the control of the neuronal extracellular space, synaptic plasticity and transmission, development and adult neurogenesis. Perineuronal glia forming groups around neurons are associated with both normal and pathological nervous tissue. Recent studies have linked reduction in the number of perineuronal oligodendrocytes in the prefrontal cortex with human schizophrenia and other psychiatric disorders. Therefore, perineuronal glia may play a decisive role in homeostasis and normal activity of the human nervous system.
Here we report on the discovery of novel cell clusters in the telencephala of five healthy Passeriforme, one Psittaciform and one Charadriiforme bird species, which we refer to as Perineuronal Glial Clusters (PGCs). The aim of this study is to describe the structure and distribution of the PGCs in a number of avian species.
PGCs were identified with the use of standard histological procedures. Heterochromatin masses visible inside the nuclei of these satellite glia suggest that they may correspond to oligodendrocytes. PGCs were found in the brains of nine New Caledonian crows, two Japanese jungle crows, two Australian magpies, two Indian mynah, three zebra finches (all Passeriformes), one Southern lapwing (Charadriiformes) and one monk parakeet (Psittaciformes). Microscopic survey of the brain tissue suggests that the largest PGCs are located in the hyperpallium densocellulare and mesopallium. No clusters were found in brain sections from one Gruiform (purple swamphen), one Strigiform (barn owl), one Trochiliform (green-backed firecrown), one Falconiform (chimango caracara), one Columbiform (pigeon) and one Galliform (chick).
Our observations suggest that PGCs in Aves are brain region- and taxon-specific and that the presence of perineuronal glia in healthy human brains and the similar PGCs in avian gray matter is the result of convergent evolution. The discovery of PGCs in the zebra finch is of great importance because this species has the potential to become a robust animal model in which to study the function of neuron-glia interactions in healthy and diseased adult brains.
doi:10.7717/peerj.110
PMCID: PMC3728766  PMID: 23904989
Perineuronal satellitosis; Oligodendroglia; Glia
23.  Optical Imaging of Retinotopic Maps in a Small Songbird, the Zebra Finch 
PLoS ONE  2010;5(8):e11912.
Background
The primary visual cortex of mammals is characterised by a retinotopic representation of the visual field. It has therefore been speculated that the visual wulst, the avian homologue of the visual cortex, also contains such a retinotopic map. We examined this for the first time by optical imaging of intrinsic signals in zebra finches, a small songbird with laterally placed eyes. In addition to the visual wulst, we visualised the retinotopic map of the optic tectum which is homologue to the superior colliculus in mammals.
Methodology/Principal Findings
For the optic tectum, our results confirmed previous accounts of topography based on anatomical studies and conventional electrophysiology. Within the visual wulst, the retinotopy revealed by our experiments has not been illustrated convincingly before. The frontal part of the visual field (0°±30° azimuth) was not represented in the retinotopic map. The visual field from 30°–60° azimuth showed stronger magnification compared with more lateral regions. Only stimuli within elevations between about 20° and 40° above the horizon elicited neuronal activation. Activation from other elevations was masked by activation of the preferred region. Most interestingly, we observed more than one retinotopic representation of visual space within the visual wulst, which indicates that the avian wulst, like the visual cortex in mammals, may show some compartmentation parallel to the surface in addition to its layered structure.
Conclusion/Significance
Our results show the applicability of the optical imaging method also for small songbirds. We obtained a more detailed picture of retinotopic maps in birds, especially on the functional neuronal organisation of the visual wulst. Our findings support the notion of homology of visual wulst and visual cortex by showing that there is a functional correspondence between the two areas but also raise questions based on considerable differences between avian and mammalian retinotopic representations.
doi:10.1371/journal.pone.0011912
PMCID: PMC2915911  PMID: 20694137
24.  Differences in number and distribution of striatal calbindin medium spiny neurons between a vocal-learner (Melopsittacus undulatus) and a non-vocal learner bird (Colinus virginianus) 
Striatal projecting neurons, known as medium spiny neurons (MSNs), segregate into two compartments called matrix and striosome in the mammalian striatum. The matrix domain is characterized by the presence of calbindin immunopositive (CB+) MSNs, not observed in the striosome subdivision. The existence of a similar CB+ MSN population has recently been described in two striatal structures in male zebra finch (a vocal learner bird): the striatal capsule and the Area X, a nucleus implicated in song learning. Female zebra finches show a similar pattern of CB+ MSNs than males in the developing striatum but loose these cells in juveniles and adult stages. In the present work we analyzed the existence and allocation of CB+ MSNs in the striatal domain of the vocal learner bird budgerigar (representative of psittaciformes order) and the non-vocal learner bird quail (representative of galliformes order). We studied the co-localization of CB protein with FoxP1, a transcription factor expressed in vertebrate striatal MSNs. We observed CB+ MSNs in the medial striatal domain of adult male and female budgerigars, although this cell type was missing in the potentially homologous nucleus for Area X in budgerigar. In quail, we observed CB+ cells in the striatal domain at developmental and adult stages but they did not co-localize with the MSN marker FoxP1. We also described the existence of the CB+ striatal capsule in budgerigar and quail and compared these results with the CB+ striatal capsule observed in juvenile zebra finches. Together, these results point out important differences in CB+ MSN distribution between two representative species of vocal learner and non-vocal learner avian orders (respectively the budgerigar and the quail), but also between close vocal learner bird families.
doi:10.3389/fnana.2013.00046
PMCID: PMC3867642  PMID: 24391552
striatum; evolution; song system; language learning; FoxP1; subventricular zone
25.  Dynamic Evolution of Base Composition: Causes and Consequences in Avian Phylogenomics 
Molecular Biology and Evolution  2011;28(8):2197-2210.
Resolving the phylogenetic relationships among birds is a classical problem in systematics, and this is particularly so when it comes to understanding the relationships among Neoaves. Previous phylogenetic inference of birds has been limited to mitochondrial genomes or a few nuclear genes. Here, we apply deep brain transcriptome sequencing of nine bird species (several passerines, hummingbirds, dove, parrot, and emu), using next-generation sequencing technology to understand features of transcriptome evolution in birds and how this affects phylogenetic inference, and combine with data from two bird species using first generation technology. The phylogenomic data matrix comprises 1,995 genes and a total of 0.77 Mb of exonic sequence. First, we find an unexpected heterogeneity in the evolution of base composition among avian lineages. There is a pronounced increase in guanine + cytosine (GC) content in the third codon position in several independent lineages, with the strongest effect seen in passerines. Second, we evaluate the effect of GC content variation on phylogenetic reconstruction. We find important inconsistencies between the topologies obtained with or without taking GC variation into account, each supporting different conclusions of past studies and also influencing hypotheses on the evolution of the trait of vocal learning. Third, we demonstrate a link between GC content evolution and recombination rate and, focusing on the zebra finch lineage, find that recombination seems to drive GC content. Although we cannot reveal the causal relationships, this observation is consistent with the model of GC-biased gene conversion. Finally, we use this unparalleled amount of avian sequence data to study the rate of molecular evolution, calibrated by fossil evidence and augmented with data from alligator transcriptome sequencing. There is a 2- to 3-fold variation in substitution rate among lineages with passerines being the most rapidly evolving and ratites the slowest. This study illustrates the potential of next-generation sequencing for phylogenomic studies but also the pitfalls when using genome-wide data with heterogeneous base composition.
doi:10.1093/molbev/msr047
PMCID: PMC3144382  PMID: 21393604
birds; phylogenetics; base composition; recombination rate; substitution rate; molecular dating

Results 1-25 (248393)