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PubMed1988

Synaptic analysis of amacrine cells with neuropeptide Y-like immunoreactivity in turtle retina.

Neuropeptide Y-like immunoreactivity has been localized previously within three classes of amacrine cells in the turtle retina. We have used the avidin-biotin with horseradish peroxidase technique to label these neurons for examination at the ultrastructural level to answer the following questions. Where are the synaptic contacts of these neurons made? What types of neurons are involved pre- and postsynaptically? What is the intracellular distribution of the immunoreactivity? Processes with neuropeptide Y-like immunoreactivity were located primarily within three regions of the inner plexiform layer: stratum 1, stratum 3, and at the border between strata 4 and 5. In all three regions the processes with neuropeptide Y-like immunoreactivity received synaptic contacts from both unlabeled amacrine and bipolar cells, but the majority of the synaptic input in all three regions was from unlabeled amacrine cells. Processes with neuropeptide Y-like immunoreactivity were presynaptic to unlabeled amacrine cells in all three regions, but also formed contacts onto unlabeled bipolar cells in the region between strata 4 and 5. The immunoreactivity within these cells gave rise to a diffuse reaction product that was distributed throughout the cytoplasm and within large vesicles. This localization of neuropeptide Y-like immunoreactivity within large vesicles suggests that this peptide may play a neuromodulatory role. Such a role would be consistent with previous studies of neuropeptides in the turtle retina.

Animals↗
PubMed1988

Organization of retinogeniculate projections in turtles of the genera Pseudemys and Chrysemys.

Organization of retinal projections to the dorsal lateral geniculate complex in turtles has been studied by means of light and electron microscopic axon tracing techniques. Orthograde degeneration studies with Fink-Heimer methods following restricted retinal lesions show the entire retina has a topologically organized projection to the contralateral dorsal lateral geniculate complex. The nasotemporal axis of the retina projects along the rostrocaudal axis of the geniculate complex; the dorsoventral axis of the retina projects along the dorsoventral axis of the geniculate complex. The projection to the ipsilateral dorsal lateral geniculate complex originates from the ventral, temporal and nasal edges of the retina. The nasotemporal axis of the ipsilateral retina projects along the rostrocaudal axis of the geniculate complex. It was not possible to determine the orientation of the dorsoventral axis of the ipsilateral retina on the geniculate complex. Light microscopic autoradiographic tracing experiments and electron microscopic degeneration experiments show the retinogeniculate projection has a laminar organization. Retinogeniculate terminals are found in both the neuropile and cell plate throughout all three subnuclei of the dorsal lateral geniculate complex but have a distinctive distribution in each subnucleus. In the subnucleus ovalis, they are frequent in both the neuropile and cell plate which forms the rostral pole of the complex. In the dorsal subnucleus, they are most prevalent in the outer part of the neuropile layer, less frequent in the inner part of the neuropile, and rare in the cell plate. In the ventral subnucleus, they are frequent in the outer part of the neuropile but are also common in the inner part of the neuropile and cell plate. These observations point to several principles of geniculate organization in turtles. First, the complex receives projections from the entire contralateral retina and a segment of the ipsilateral retina. It thus has monocular and binocular segments that together receive a topologically organized representation of the binocular visual space and the contralateral monocular visual space. Second, the three geniculate subnuclei receive information from different, specialized regions of the retina and visual space. Subnucleus ovalis receives information from the frontal binocular visual field. The ventral subnucleus receives information from the caudal binocular field. The dorsal subnucleus receives input from the contralateral monocular field. Third, there is a lamination of retinal inputs in the geniculate complex which differs in character within the three subnuclei.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed1988

Auditory receptor of the red-eared turtle: II. Afferent and efferent synapses and innervation patterns.

Innervation patterns in the auditory receptor of the red-eared turtle were reconstructed from serial ultrathin sections. Four locations were studied, including three on the basilar membrane and one on the basal limbus. In that area of the papilla located above the apical end of the basilar membrane most cells were innervated by single afferent fibers which, in turn, supplied as many as three cells. Although afferents in the midmembrane area of the papilla supplied fewer cells, the innervation pattern was similar in other respects to that in the apical area including an abundance of efferent synapses on afferents. In contrast, hair cells in the basal membrane area were contacted by two afferent fibers and had five times as many afferent synapses as observed previously. Here, each afferent made twice as many synapses as fibers in the previous two areas and supplied one or two hair cells but received no efferent synapses. In the basal limbus area, each hair cell was contacted by as many as eight afferents and each afferent supplied as many as seven hair cells. The significance of these innervation patterns is discussed in the light of structural information obtained from other vertebrate auditory receptors and in the light of available functional information derived from the turtle papilla.

Animals↗
PubMed1990

Telodendrial contact of HRP-filled photoreceptors in the turtle retina: pathways of photoreceptor coupling.

Synaptic contacts of photoreceptors in the turtle retina were studied by intracellular injection of horseradish peroxidase (HRP) and electron microscopy. Both cone and rod photoreceptors radiated basal processes (telodendria) from their terminal endings. These telodendria ran laterally in the outer plexiform layer. The telodendria of cones gave rise to many fine branches that penetrated synaptic cavities of several neighboring cones. Tips of these branches terminated near the walls of synaptic cavities. Some of the telodendrial contact formed two types of basal junction: symmetrical and punctate. The distribution of cones that made telodendrial contacts with the HRP-filled cone were quantitatively investigated. Green-sensitive cones (n = 3) made telodendrial contacts with neighboring red- and blue-sensitive cones, blue-sensitive cones (n = 4) with red- and green-sensitive cones, and red-sensitive cones (n = 9) with red- and green-sensitive cones. In contrast to these cone connections, rod telodendria did not penetrate neighboring photoreceptors. Direct synaptic contacts were not found between rods and cones. Our results clarify the variety of cone couplings in turtle retina: the three chromatic classes of cones are selectively coupled by the basal junctions at the ends of telodendrial processes.

Animals↗
PubMed1990

Spatial organization of axons in turtle visual cortex: intralamellar and interlamellar projections.

The spatial pattern of projections within turtle visual cortex was studied by using focal injections of horseradish peroxidase into visual cortex in an in vitro wholebrain preparation. Injections anterogradely filled the axons of many layer 2 neurons, which could be followed for 200-500 microns from the injection sites. Axons were typically unbranched, relatively straight, and bore small varicosities at irregular intervals. They radiated from the injection sites in all directions, but showed some preference toward orientations along the lateral-medial axis of the cortex. Earlier work (Mulligan and Ulinski, '90) had demonstrated that turtle visual cortex contains a series of isoazimuth lamellae, each representing an individual azimuth of visual space and oriented perpendicular to the rostral-caudal axis of the cortex. The present study provides evidence for intrinsic projections both along isoazimuth lamellae and between adjacent lamellae. These projections may play roles in the elaboration of wide receptive fields of cortical neurons.

Animals↗
PubMed1991

Localization of aspartate-like immunoreactivity in the retina of the turtle (Pseudemys scripta).

Aspartate has been reported to be a putative excitatory neurotransmitter in the retina, but little detailed information is available concerning its anatomical distribution. We used an antiserum directed against an aspartate-albumin conjugate to analyze the anatomy, dendritic stratification, and regional distribution of cell types with aspartate-like immunoreactivity in the turtle retina. The results showed dramatic differences in immunoreactivity in the peripheral versus the central retina. Strong aspartate-like immunoreactivity was shown in the peripheral retina, with many well-labeled processes in the inner plexiform layer. Many bipolar, horizontal, amacrine, and ganglion cells, some photoreceptors, and some unidentified cells were strongly immunoreactive in the peripheral retina. In contrast, although the central retina showed well-labeled horizontal cells, there was only light labeling in the inner plexiform layer with weakly immunoreactive amacrine and ganglion cells and no labeled bipolar cells. There were several strongly immunoreactive efferent nerve fibers which left the optic nerve head and arborized extensively in the retina. At the electron microscopic level, electron-dense reaction product was associated with synaptic vesicles at bipolar and amacrine cell synapses in the inner plexiform layer. These results suggest that aspartate may be involved in many diverse synaptic interactions in both the outer plexiform layer and the inner plexiform layer of the turtle retina.

Animals↗
PubMed1992

Monoaminergic systems in the brainstem and spinal cord of the turtle Pseudemys scripta elegans as revealed by antibodies against serotonin and tyrosine hydroxylase.

With the aim of gaining more insight into the monoaminergic regulation of spinal motor systems in the turtle, we have studied the distribution of 5-HT (5-HTir) and tyrosine hydroxylase immunoreactivity (THir) in the brainstem and spinal cord of Pseudemys scripta elegans. 5-HTir cell bodies were located in the midline in nucleus raphe inferior, nucleus raphe superior, and laterally in nuclei reticularis superior and inferior and nucleus reticularis isthmi. THir cell bodies were located in the commissural nucleus, nucleus tractus solitarii, the locus coeruleus-subcoeruleus complex, nuclei reticularis superior and inferior, the pretectal area, and substantia nigra. 5-HTir and THir tracts were found in lateral and ventral bundles superficially in the brainstem. 5-HTir fibers in the spinal cord were located in a large dorsolateral and a smaller ventrolateral tract. In the gray matter, a high concentration of 5-HTir fibers were observed in areas I-IV and in the lateral motor column of cervical and lumbar enlargements. Areas V-VIII and area X were less intensively innervated, with the lowest fibre concentration in areas VII-VIII and area X. Throughout the spinal cord, THir nerve fibres were located in the same areas but with a lower density. Small bipolar 5-HTir and THir cell bodies were found ventromedially to the central canal especially in cervical and lumbosacral segments. Large THir cells were found in area IX in the caudal sacral and coccygeal spinal cord. THir cerebrospinal fluid-contacting cells were also found in the most caudal part of the brainstem and the upper cervical spinal cord. The well developed spinal 5-HT system and the less developed THir system provides an anatomical explanation for the monoaminergic modulation of turtle motoneuron membrane properties, which has been observed in electrophysiological experiments.

Animals↗
PubMed1994

Descending propriospinal axons in the hindlimb enlargement of the red-eared turtle: cells of origin and funicular courses.

Spinal neurons with descending axons are important components of spinal sensorimotor networks. We used an anatomical tracing technique to study the distribution of descending propriospinal axons and cell bodies in red-eared turtles. We injected horseradish peroxidase into a portion of one funiculus in the middle of the hindlimb enlargement and examined six spinal segments rostral to the injection site (dorsal 3 through dorsal 8) for labeled neuronal cell bodies. Injections into each region of the white matter labeled substantial numbers of descending propriospinal neurons. Each injection labeled cell bodies over most of the six spinal segments examined. Each injection also labeled cell bodies in the ipsilateral dorsal horn, intermediate zone, and ventral horn as well as the contralateral intermediate zone and ventral horn. Injections into each of four regions of the white matter, the dorsal funiculus, the medial part of the lateral funiculus, the lateral part of the lateral funiculus, and the ventral funiculus reliably gave rise to a distinct distribution of labeled cell bodies. These experiments establish that descending propriospinal axons in red-eared turtles are found in all regions of the spinal white matter. This finding contrasts with a popular contemporary view of the organization of descending propriospinal axons in mammals. These experiments also demonstrate that neurons in each region of the gray matter give rise to a different distribution of descending, funicular axons, although these distributions are widely overlapping. Different funicular axon distributions could be associated with different sets of synaptic contacts with the white-matter dendrites of spinal neurons.

Animals↗
PubMed1994

Distribution of galanin-like immunoreactivity in the brain of the turtle Mauremys caspica.

Galanin is a brain-gut peptide present in the central nervous system of fish, amphibians, birds, and mammals. For comparative studies among vertebrates, the distribution of galanin in the brain of reptiles has been investigated. We studied the localization of galanin-like-immunoreactive perikarya and nerve fibers in the brain of the turtle Mauremys caspica by using an antiserum against porcine galanin. In the telencephalon, few immunoreactive perikarya were seen in the amygdaloid complex. The diencephalon contained the majority of the immunoreactive perikarya present in the lamina terminalis, nucleus periventricularis anterior, lateral preoptic area, nuclei hypothalamicus ventromedialis and posterior, nucleus basalis of the anterior commissure, and nucleus ventralis tuberis. Many immunoreactive cells, especially in the infundibulum, contacted the cerebrospinal fluid by an apical process. In the rhombencephalon, immunopositive perikarya were restricted to a few cells in the nucleus tractus solitari. In the mesencephalon, they were absent. Immunoreactive nerve fibers were present in all regions containing labeled perikarya and in 1) telencephalon: septum, nucleus fasciculi diagonalis Brocae; 2) diencephalon: nucleus paraventricularis, nucleus supraopticus, nucleus suprachiasmaticus, subventricular grey, nucleus of the paraventricular organ, nucleus mamillaris, infundibular decussation, outer layer of the median eminence, posterior commissure and subcommissural organ region, habenula, nuclei dorsomedialis anterior, and dorsolateralis anterior of the thalamus; and 3) mesencephalon and rhombencephalon: stratum griseum periventriculare, stratum fibrosum periventriculare, laminar nucleus of the torus semicircularis, periventricular grey, nucleus interpeduncularis, nucleus ruber, substantia nigra, locus coeruleus, raphe nuclei, nuclei of the reticular formation, nucleus motorius nervi trigemini, cochlear and vestibular area, and nucleus spinalis nerve trigemini. Our results suggest that galanin may have hypophysiotropic and central roles in the turtle Mauremys caspica.

Animals↗
PubMed1995

The organization of the turtle inner retina. I. ON- and OFF-center pathways.

Intracellular recordings and dye injections of Lucifer yellow, horseradish peroxidase, or Neurobiotin were made in bipolar, amacrine, and ganglion cells of the Pseudemys turtle retina. By using a standard light-stimulation protocol in a sample of 375 labeled neurons, we were able to identify morphological and physiological characteristics of 11 types of bipolar cell, 37 types of amacrine cell, and 24 types of ganglion cell. To make sense of these data, we have chosen to group the 72 essentially different neuron types into traditional, functionally significant pathways. In this paper we look at the neuronal types in the inner plexiform layer (IPL) in terms of their contribution to generalized luminosity responses such as sustained ON- or OFF-center and transient ON-OFF ganglion cells; in the companion paper (J. Ammermüller, J.F. Muller, and H. Kolb, 1995, J. Comp. Neurol. 358:35-62) we look at them in terms of their involvement in color opponency and directional selectivity. A functional organization of the turtle IPL into OFF sublaminae (strata 1 and 2) and ON sublaminae (strata 3, 4, and 5), as has been described for other vertebrate retinas, was quite clear for two varieties of OFF-center bipolar cells (B4 and B5) and for all four types of sustained ON-center bipolar cell (B1, B2, B6, and B7). Thus, we found no sustained ON-center bipolar cell terminating in strata 1 and 2. We did, however, see three varieties of sustained OFF-center bipolar cells (B3, B9, and B10) having axon terminals in strata 3-5 (the ON sublamina) in addition to their terminations in stratum 1 or 2 (the OFF sublamina). Monostratified sustained ON- and OFF-center amacrine and ganglion cells rigidly obeyed the border of ON and OFF sublaminae. However, multistratified and diffuse sustained amacrine and ganglion cells could be either ON-center or OFF-center, and they did not strictly obey the border: such ON-center cells always had processes in one of the ON sublaminae (strata 3-5), and the equivalent OFF-center cells always had processes in one of the OFF sublaminae (strata 1 and 2). Monostratified transient amacrine and ganglion cells were concentrated in the middle of the IPL (around stratum 3), whereas bi-, tri-, or multistratified transient amacrine or ganglion cells always had processes in both the ON and the OFF sublaminae.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed2001

Evidence for the neural crest origin of turtle plastron bones.

The migrating cranial neural crest cells of birds, fish, and mammals have been shown to form the membranous bones of the cranium and face. These findings have been extrapolated to suggest that all the dermal bones of the vertebrate exoskeleton are derived from the neural crest ectomesenchyme. However, only one group of extant animals, the Chelonians, has an extensive bony exoskeleton in the trunk. We have previously shown that the autapomorphic carapacial and plastron bones of the turtle shell arise from dermal intramembranous ossification. Here, we show that the bones of the plastron stain positively for HNK-1 and PDGFRalpha and are therefore most likely of neural crest origin. This extends the hypothesis of the neural crest origin of the exoskeleton to include the turtle plastron.

Animals↗
PubMed2007

Immunohistochemical and hodological characterization of calbindin-D28k-containing neurons in the spinal cord of the turtle, Pseudemys scripta elegans.

Neurons and fibers containing the calcium-binding protein calbindin-D28k (CB) were studied by immunohistochemical techniques in the spinal cord of adult and juvenile turtles, Pseudemys scripta elegans. Abundant cell bodies and fibers immunoreactive for CB were widely and distinctly distributed throughout the spinal cord. Most neurons and fibers were labeled in the superficial dorsal horn, but numerous cells were also located in the intermediate gray and ventral horn. In the dorsal horn, most CB-containing cells were located in close relation to the synaptic fields formed by primary afferents, which were not labeled for CB. Double immunohistofluorescence demonstrated distinct cell populations in the dorsal horn labeled only for CB or nitric oxide synthase, whereas in the dorsal part of the ventral horn colocalization of nitric oxide synthase was found in about 6% of the CB-immunoreactive cells in this region. Choline acetyltransferase immunohistochemistry revealed that only about 2% of the neurons in the dorsal part of the ventral horn colocalized CB, whereas motoneurons were not CB-immunoreactive. The involvement of CB-containing neurons in ascending spinal projections to the thalamus, tegmentum, and reticular formation was demonstrated combining the retrograde transport of dextran amines and immunohistochemistry. Similar experiments demonstrated supraspinal projections from CB-containing cells mainly located in the reticular formation but also in the thalamus and the vestibular nucleus. The revealed organization of the neurons and fibers containing CB in the spinal cord of the turtle shares distribution and developmental features, colocalization with other neuronal markers, and connectivity with other tetrapods and, in particular with mammals.

Animals↗
PubMed2001

Sex reversal and aromatase in the European pond turtle: treatment with letrozole after the thermosensitive period for sex determination.

In the European pond turtle (Emys orbicularis), gonadal sex differentiation is temperature-dependent. The temperature sensitive period (TSP) of gonadogenesis lies between stages 16 and 22 of embryonic development. Previous studies have shown that embryos incubated at 30 degrees C, a temperature yielding 100% phenotypic females, can be sex reversed by treatments with an aromatase inhibitor administered during TSP or even somewhat after TSP (as of stage 22+). The goal of the present study was to determine whether the ovary still retains male potential at later stages of embryonic development and whether the induced male characters persist after hatching. For this purpose, eggs of E. orbicularis were treated with letrozole, a nonsteroidal aromatase inhibitor, at or as of stages 23, 24 or 25, then gonadal aromatase activity in each individual and the related gonadal structure were studied at hatching (stage 26) and for one year after hatching. Two kinds of treatments were carried out: 1) repeated applications of 10 microg of letrozole in ethanolic solution onto the eggshell; and 2) a single injection of 10 microg of letrozole in olive oil. Similar results were obtained with either application or injection of the aromatase inhibitor. In treatments as of or at stage 23, individuals with gonadal aromatase activity lower than 20 fmoles/hour/gonad had ovotestes, i.e., 22% of the treated individuals. At hatching, the inner part of these ovotestes contained testicular cords and also mixed lacunae presenting various degrees of transdifferentiation of the epithelium into a Sertolian epithelium. The cortex was maintained, although some germ cells degenerated within it. These processes continued after hatching. However, at 12 months, gonads were still ovotestes displaying some follicles with a growing oocyte in the remaining parts of the cortex. In treatments as of or at stages 24 or 25, only a few individuals were masculinized. One had ovotestes; in others, the cortex was absent in some parts and when it was present oocytes were degenerating. These results show that in the European pond turtle, differentiation of ovotestes from ovaries can be induced by treatment with an aromatase inhibitor starting at late stages of embryonic development (between the end of TSP and hatching), although such differentiation is less frequent as embryonic development proceeds. Sex reversal persists for at least one year after hatching. J. Exp. Zool. 290:490-497, 2001.

Animals↗
PubMed2001

Development of an evolutionarily novel structure: fibroblast growth factor expression in the carapacial ridge of turtle embryos.

The turtle shell, an evolutionarily novel structure, contains a bony exoskeleton that includes a dorsal carapace and a ventral plastron. The development of the carapace is dependent on the carapacial ridge (CR), a bulge in the dorsal flank that contains an ectodermal structure analogous to the apical ectodermal ridge (AER) of the developing limb (Burke. 1989a. J Morphol 199:363-378; Burke. 1989b. Fortschr Zool 35:206-209). Although the CR is thought to mediate the initiation and outgrowth of the carapace, the mechanisms of shell development have not been studied on the molecular level. Here, we present data suggesting that carapace formation is initiated by co-opting genes that had other functions in the ancestral embryo, specifically those of limb outgrowth. However, there is divergence in the signaling repertoire from that involved in limb initiation and outgrowth. In situ hybridizations with antisense riboprobes derived from Trionyx spiniferous fibroblast growth factor-10 (tfgf10) and Trachemys scripta (T. scripta) fibroblast-growth factor 8 (tfgf8) cDNAs were performed on sections of early T. scripta embryos (< 30 days). Expression of tfgf10 was localized to the mesenchyme subjacent to the ectoderm of the CR. In the chick limb bud, FGF10 is known to be expressed in the early limb-forming mesenchyme and is capable of inducing FGF8 in the AER to initiate the outgrowth of the limb bud. Although the expression of tfgf8 was found in the AER of the developing turtle limb, it was not seen in the CR. Thus, the initiation of the carapace is in agreement with FGF10 expression in the CR, but FGF8 does not appear to have a role in mediating early carapace outgrowth.

Animals↗
PubMed2002

Sperm storage in turtles: A male perspective.

The storage and behavior of sperm collected from the epididymis of two emyiid turtles were examined. In Chrysemys picta, the weight of the epididymis does not change significantly throughout the year as does the testis. However, in this species, as well as in Trachemys scripta, the epididymis contains sperm throughout the entire year. Sperm from both species have a relatively low motility and velocity of movement. In C. picta, equally low motilities are observed both in the autumn, shortly after spermiation, and in spring. Motility could be augmented by the addition of isobutyl methyl xanthine (IBMX, 0.5 mmol l(-1)). Epididymal sperm remained viable in excess of 40 days in vitro when stored in F-10 buffer, during which time motility and swimming velocity could be augmented with IBMX. The longevity and low motility of turtle sperm facilitates its storage by either males or females, and creates conditions that promote the wide dissemination, over time, of gametes produced in a narrow time window.

Adaptation, Physiological↗
PubMed1978

Structure, function, and long-term maintenance of the isolated turtle colon.

We describe the 5-day maintenance of sacs of turtle colonic mucosa in enriched bathing solutions. The mean maximum transepithelial potential difference (PD) developed by the sacs in Ringer solution enriched with tissue-culture medium and gassed with 95% air-5% CO2 was 126 mV at 24 hours. Lower values were observed in other solutions. The PD of 24-hour sacs was partially or totally inhibited by ouabain, replacement of Na by choline in mucosal bathing fluids, or removal of Ca from serosal bathing fluids. The sacs transported Na in excess of H2O forming a dilute mucosal solution. The response of four different sac preparations (normally oriented or everted, and stripped normally oriented or everted) to long incubation were compared. Stripped normally oriented tissue developed the highest PD and maintained the lowest water content. The morphology of fresh and long-incubated tissue was examined. This investigation demonstrates that the turtle colon can be maintained in vitro for long periods, and it provides information on the morphology and physiology of this tissue.

Animals↗
PubMed1995

Peptidergic and adrenergic innervation of the lachrymal gland in the euryhaline turtle, Malaclemys terrapin.

The controlling factors of lachrymal gland secretions were examined in the euryhaline turtle, Malaclemys terrapin. Histochemical and immunocytochemical methods were used to localize some of the possible neurotransmitters involved. There was no immunoreactivity to choline acetyltransferase, the enzyme synthesizing acetylcholine, nor did the histochemical technique for acetylcholinesterase produce positive results. Immunofluorescence and immunoperoxidase labels revealed vasoactive intestinal peptide (VIP)- and neuropeptide Y (NPY)-like immunoreactivity in high concentrations surrounding the secretory tubules and ducts. Substance P produced a weak immunoreactivity in the interstitial space surrounding the ducts. Dopamine beta-hydroxylase, the enzyme synthesizing norepinephrine and epinephrine, was localized around the blood vessels. Immunogold labeling confirmed the presence of VIP- and NPY-like reactivity in nerve varicosities close to the basement membrane of the secretory epithelium, and double-labeling showed VIP and NPY are co-localized within the same nerve terminals. The results suggest that the secretory epithelium may be primarily under peptidergic control while the vascular system is under adrenergic control. This is possibly a new pattern of innervation for exocrine glands and may be related to the particular function of this salt gland in an euryhaline turtle.

Acetylcholinesterase↗
PubMed2005

How the turtle forms its shell: a paracrine hypothesis of carapace formation.

We propose a two-step model for the evolutionary origin of the turtle shell. We show here that the carapacial ridge (CR) is critical for the entry of the ribs into the dorsal dermis. Moreover, we demonstrate that the maintenance of the CR and its ability to attract the migrating rib precursor cells depend upon fibroblast growth factor (FGF) signaling. Inhibitors of FGF allow the CR to degenerate, with the consequent migration of ribs along the ventral body wall. Beads containing FGF10 can rearrange rib migration in the chick, suggesting that the CR FGF10 plays an important role in attracting the rib rudiments. The co-ordinated growth of the carapacial plate and the ribs may be a positive feedback loop (similar to that of the limbs) caused by the induction of Fgf8 in the distal tips of the ribs by the FGF10-secreting mesenchyme of the CR. Once in the dermis, the ribs undergo endochrondral ossification. We provide evidence that the ribs act as signaling centers for the dermal ossification and that this ossification is due to bone morphogenetic proteins secreted by the rib. Thus, once the ribs are within the dermis, the ossification of the dermis is not difficult to achieve. This relatively rapid means of carapace formation would allow for the appearance of turtles in the fossil record without obvious intermediates.

Animals↗