Skull and brain of a 300-million-year-old chimaeroid fish revealed by synchrotron holotomography

Pradel, Alan; Langer, Max; Maisey, John G.; Geffard-Kuriyama, Didier; Cloetens, Peter; Janvier, Philippe; Tafforeau, Paul

doi:10.1073/pnas.0807047106

Cited by 83 publications

(72 citation statements)

References 29 publications

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“…One particularly successful implementation of quantitative inline phase contrast is a technique known as holotomography, in which images recorded at several distances behind the specimen are combined to quantitatively retrieve the phase shift (Cloetens et al 1999). A prominent, recent example is the imaging of a fossilized fish (Pradel et al 2009), containing the only known three-dimensional representation of a fossilized brain so far. The third approach, particularly relevant for soft tissues, is analyser-based imaging (ABI).…”

Section: Introductionmentioning

confidence: 99%

High-resolution tomographic imaging of a human cerebellum: comparison of absorption and grating-based phase contrast

Schulz

Weitkamp

Zanette

et al. 2010

J. R. Soc. Interface.

142

110

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Human brain tissue belongs to the most impressive and delicate three-dimensional structures in nature. Its outstanding functional importance in the organism implies a strong need for brain imaging modalities. Although magnetic resonance imaging provides deep insights, its spatial resolution is insufficient to study the structure on the level of individual cells. Therefore, our knowledge of brain microstructure currently relies on two-dimensional techniques, optical and electron microscopy, which generally require severe preparation procedures including sectioning and staining. X-ray absorption microtomography yields the necessary spatial resolution, but since the composition of the different types of brain tissue is similar, the images show only marginal contrast. An alternative to absorption could be X-ray phase contrast, which is known for much better discrimination of soft tissues but requires more intricate machinery. In the present communication, we report an evaluation of the recently developed X-ray grating interferometry technique, applied to obtain phase-contrast as well as absorption-contrast synchrotron radiation-based microtomography of human cerebellum. The results are quantitatively compared with synchrotron radiationbased microtomography in optimized absorption-contrast mode. It is demonstrated that grating interferometry allows identifying besides the blood vessels, the stratum moleculare, the stratum granulosum and the white matter. Along the periphery of the stratum granulosum, we have detected microstructures about 40 mm in diameter, which we associate with the Purkinje cells because of their location, size, shape and density. The detection of individual Purkinje cells without the application of any stain or contrast agent is unique in the field of computed tomography and sets new standards in non-destructive three-dimensional imaging.

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Section: Introductionmentioning

confidence: 99%

High-resolution tomographic imaging of a human cerebellum: comparison of absorption and grating-based phase contrast

Schulz

Weitkamp

Zanette

et al. 2010

J. R. Soc. Interface.

142

110

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“…Brain tissues are among the least commonly preserved soft tissues in the fossil record because fossilized brains themselves are extremely rare and, more importantly, because most brain tissues are highly labile. The vast majority of our knowledge of the brains of ancient organisms comes not from preserved brain tissue (although see Pradel et al 2009), but from indirect sources. These include comparative anatomical studies of closely related extant taxa, the study of fossilized endocasts (the natural internal casts of braincases; e.g.…”

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confidence: 99%

“…More recently, imaging techniques such as tomography have been used to create accurate three-dimensional representations of endocranial cavities in a variety of dinosaurs (Rogers 1999;Brochu 2000;Witmer et al 2008;Lautenschlager et al 2012), as well as other fossil taxa extending back into the Palaeozoic (e.g. Pradel et al 2009;Giles & Friedman 2014;Marek et al 2015).…”

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confidence: 99%

Remarkable preservation of brain tissues in an Early Cretaceous iguanodontian dinosaur

Brasier

Norman

Liu

et al. 2016

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It has become accepted in recent years that the fossil record can preserve labile tissues. We report here the highly detailed mineralization of soft tissues associated with a naturally occurring brain endocast of an iguanodontian dinosaur found in c. 133 Ma fluvial sediments of the Wealden at Bexhill, Sussex, UK. Moulding of the braincase wall and the mineral replacement of the adjacent brain tissues by phosphates and carbonates allowed the direct examination of petrified brain tissues. Scanning electron microscopy (SEM) imaging and computed tomography (CT) scanning revealed preservation of the tough membranes (meninges) that enveloped and supported the brain proper. Collagen strands of the meningeal layers were preserved in collophane. The blood vessels, also preserved in collophane, were either lined by, or infilled with, microcrystalline siderite. The meninges were preserved in the hindbrain region and exhibit structural similarities with those of living archosaurs. Greater definition of the forebrain (cerebrum) than the hindbrain (cerebellar and medullary regions) is consistent with the anatomical and implied behavioural complexity previously described in iguanodontian-grade ornithopods. However, we caution that the observed proximity of probable cortical layers to the braincase walls probably resulted from the settling of brain tissues against the roof of the braincase after inversion of the skull during decay and burial.

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“…A hyoid ray-supported opercular flap has been reported in the symmoriid Falcatus (36) (hyoid rays reported after reexamination in ref. 8), and has also been described in certain iniopterygians (37,38), although there is evidence that these groups may be stem holocephalans (8,11,12,39,40). With such variation documented in only a small number of known taxa, a thorough reevaluation of chondrichthyan phylogeny and pharyngeal endoskeletal anatomy is clearly needed to accurately reconstruct the frequency, timing, and polarity of chondrichthyan branchial ray expansion and reduction.…”

Section: Discussionmentioning

confidence: 99%

Holocephalan embryos provide evidence for gill arch appendage reduction and opercular evolution in cartilaginous fishes

Gillis

Rawlinson²,

Bell³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Chondrichthyans possess endoskeletal appendages called branchial rays that extend laterally from their hyoid and gill-bearing (branchial) arches. Branchial ray outgrowth, like tetrapod limb outgrowth, is maintained by Sonic hedgehog (Shh) signaling. In limbs, distal endoskeletal elements fail to form in the absence of normal Shh signaling, whereas shortened duration of Shh expression correlates with distal endoskeletal reduction in naturally variable populations. Chondrichthyans also exhibit natural variation with respect to branchial ray distribution-elasmobranchs (sharks and batoids) possess a series of ray-supported septa on their hyoid and gill arches, whereas holocephalans (chimaeras) possess a single hyoid arch raysupported operculum. Here we show that the elongate hyoid rays of the holocephalan Callorhinchus milii grow in association with sustained Shh expression within an opercular epithelial fold, whereas Shh is only transiently expressed in the gill arches. Coincident with this transient Shh expression, branchial ray outgrowth is initiated in C. milii but is not maintained, yielding previously unrecognized vestigial gill arch branchial rays. This is in contrast to the condition seen in sharks, where sustained Shh expression corresponds to the presence of fully formed branchial rays on the hyoid and gill arches. Considered in light of current hypotheses of chondrichthyan phylogeny, our data suggest that the holocephalan operculum evolved in concert with gill arch appendage reduction by attenuation of Shhmediated branchial ray outgrowth, and that chondrichthyan branchial rays and tetrapod limbs exhibit parallel developmental mechanisms of evolutionary reduction.

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Skull and brain of a 300-million-year-old chimaeroid fish revealed by synchrotron holotomography

Cited by 83 publications

References 29 publications

High-resolution tomographic imaging of a human cerebellum: comparison of absorption and grating-based phase contrast

High-resolution tomographic imaging of a human cerebellum: comparison of absorption and grating-based phase contrast

Remarkable preservation of brain tissues in an Early Cretaceous iguanodontian dinosaur

Holocephalan embryos provide evidence for gill arch appendage reduction and opercular evolution in cartilaginous fishes

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