Fig 18 - uploaded by Jacques Repérant
Content may be subject to copyright.
Photomicrograph of transverse section through the optic tectum, normal material, Fink-Heimer preparation. x 120. Fig. 19. Photomicrograph of transverse section through the mid-medial optic tecta 30 days after right retinal ablation. Note the absence of degenerated optic fibers in the ipsilateral tractus opticus marginalis pars medialis (TOMi). ~260. Fig. 20. Brightfield radioautograph showing labeling in the contralateral optic tectum 5 days after intraocular injection 01 :I combined solution of ['Hlproline and ['H)fucosc. x 110.
Source publication
The retinal projections of the shark Scyliorhinus canicula were investigated using both the degeneration technique after eye removal and the radioautographic method following the intraocular injection of various tritiated tracers (proline, leucine, fucose, adenosine). The results showed contralateral projection via different optic tract components...
Citations
... These brain nuclei were also analyzed using the FIF method (Wilson and Dodd, 1973b;Molist et al., 1993;Rodríguez-Moldes et al., 1993) and immunohistochemistry against dopamine, which was specifically carried out on the thorny skate Ambliraja radiata (Meredith and Smeets, 1987). Notably, due to its topography, SCN may be involved in the primary visual pathways (Repérant et al., 1986;Northcutt, 1990), revealing DAminergic somata (Meredith and Smeets, 1987) or fairly FIF+ somata and projecting its CAminergic axons to the NIL (Wilson and Dodd, 1973b;Molist et al., 1993). Moreover, the existent descriptions of CAminergic PO share the presence of FIF+, TH+, and DA+ neurons, which are mostly scattered under the floor of the third ventricle (Wilson and Dodd, 1973b;Meredith and Smeets, 1987;Rodriguez-Moldes and Anadon, 1987;Stuesse et al., 1990Stuesse et al., , 1991Stuesse et al., , 1994Molist et al., 1993;Rodríguez-Moldes et al., 1993;Carrera et al., 2012). ...
... On the other hand, our results did not show significant differences in cell number between the developing F2 stage and the mature ones, showing the same pattern. In S. canicula, the suprachiasmatic nucleus (SCN) is both a primary (Repérant et al., 1986;Northcutt, 1990) and a secondary visual region (Wilson and Dodd, 1973b;Wilson et al., 1974). Additionally, its CAminergic component may exert inhibitory control over the release of melanocyte-stimulating hormone in NIL, as well as integrating impulses from light reflected off the environmental background and regulating the skin paling of the catshark (Wilson and Dodd, 1973a,b;Wilson et al., 1974;Molist et al., 1993;Carrera et al., 2012). ...
Introduction: The catecholaminergic component of the brain-pituitary-gonadal axis, which mediates the influence of external and internal stimuli on the central nervous system and gonad development in vertebrates, is largely unexplored in Chondrichthyes. We considered Scyliorhinus canicula (L., 1758) females as a model for this vertebrate's class, to assess the involvement of the catecholaminergic system of the brain in its reproduction. Along the S. canicula reproductive cycle, we characterized and evaluated differences in somata morphometry and the number of putative catecholaminergic neurons in two brain nuclei: the periventricular preoptic nucleus, hypothesized to be a positive control for ovarian development, and the suprachiasmatic nucleus, examined as a negative control.
Materials and methods: 16 S. canicula wild females were sampled and grouped in maturity stages (immature, maturing, mature, and mature egg-laying). The ovary was histologically processed for the qualitative description of maturity stages. Anti-tyrosine hydroxylase immunofluorescence was performed on the diencephalic brain sections. The immunoreactive somata were investigated for morphometry and counted using the optical fractionator method, throughout the confocal microscopy.
Results and discussions: Qualitative and quantitative research confirmed two separate populations of immunoreactive neurons. The modifications detected in the preoptic nucleus revealed that somata were more numerous, significantly smaller in size, and more excitable during the maturing phase but decreased, becoming slightly bigger and less excitable in the egg-laying stage. This may indicate that the catecholaminergic preoptic nucleus is involved in the control of reproduction, regulating both the onset of puberty and the imminent spawning. In contrast, somata in the suprachiasmatic nucleus grew in size and underwent turnover in morphometry, increasing the total number from the immature-virgin to maturing stage, with similar values in the more advanced maturity stages. These changes were not linked to a reproductive role. These findings provide new valuable information on Chondrichthyes, suggesting the existence of an additional brain system implicated in the integration of internal and environmental cues for reproduction.
... More recently, a method for genetic manipulation has become available [47]. Over the years, S. canicula proved to be a valid and good model for the study of a lot of biological processes, such as brain development [48][49][50], lifelong tooth cycling [44,51], retina function and development [52][53][54], and the immune system [55][56][57][58]. We therefore decided to investigate the distribution of neurotrophin genes by in situ hybridization in the brain of the small spotted catshark. ...
Neurotrophins (NTFs) are structurally related neurotrophic factors essential for differentiation , survival, neurite outgrowth, and the plasticity of neurons. Abnormalities associated with neurotrophin-signaling (NTF-signaling) were associated with neuropathies, neurodegenerative disorders , and age-associated cognitive decline. Among the neurotrophins, brain-derived neurotrophic factor (BDNF) has the highest expression and is expressed in mammals by specific cells throughout the brain, with particularly high expression in the hippocampus and cerebral cortex. Whole genome sequencing efforts showed that NTF signaling evolved before the evolution of Vertebrates; thus, the shared ancestor of Protostomes, Cyclostomes, and Deuterostomes must have possessed a single ortholog of neurotrophins. After the first round of whole genome duplication that occurred in the last common ancestor of Vertebrates, the presence of two neurotrophins in Agnatha was hypothesized, while the monophyletic group of cartilaginous fishes, or Chondrichthyans, was situated immediately after the second whole genome duplication round that occurred in the last common ancestor of Gnathostomes. Chondrichthyans represent the outgroup of all other living jawed vertebrates (Gnathostomes) and the sister group of Osteichthyans (comprehensive of Actinopterygians and Sarcopterygians). We were able to first identify the second neurotrophin in Agnatha. Secondly, we expanded our analysis to include the Chondrichthyans, with their strategic phylogenetic position as the most basal extant Gnathostome taxon. Results from the phylogenetic analysis confirmed the presence of four neurotrophins in the Chondrichthyans, namely the orthologs of the four mammalian neurotrophins BDNF, NGF, NT-3, and NT-4. We then proceeded to study the expression of BDNF in the adult brain of the Chondrichthyan Scyliorhinus canicula. Our results showed that BDNF is highly expressed in the S. canicula brain and that its expression is highest in the Telencephalon, while the Mesencephalic and Diencephalic areas showed expression of BDNF in isolated and well-defined cell groups. NGF was expressed at much lower levels that could be detected by PCR but not by in situ hybridization. Our results warrant further investigations in Chondrichthyans to characterize the putative ancestral function of neurotrophins in Vertebrates.
... Experimental studies in catshark reported that optic tectum receives a major retinal projection on external tectal layers (Repérant et al., 1986;Smeets, 1981), as in most vertebrates. The catshark optic tectum also receives afferents from various brain nuclei and regions extending from the pallium to the spinal cord (Smeets, 1982) tum, and some of them exhibit radial dendrites coursing through two or more layers (Manso & Anadon, 1991), but ascription of PSST+ cells to these cell types is not possible. ...
Five prosomatostatin genes (PSST1, PSST2, PSST3, PSST5 and PSST6) have been recently identified in elasmobranchs (Tostivint, Gaillard, Mazan, & Pézeron, 2019). In order to gain insight into the contribution of each somatostatin to specific nervous systems circuits and behaviors in this important jawed vertebrate group, we studied the distribution of neurons expressing PSST mRNAs in the central nervous system (CNS) of Scyliorhinus canicula using in situ hybridization. Additionally, we combined in situ hybridization with tyrosine hydroxylase (TH) immunochemistry for better characterization of PSST1 and PSST6 expressing populations. We observed differential expression of PSST1 and PSST6, which are the most widely expressed PSST transcripts, in cell populations of many CNS regions, including the pallium, subpallium, hypothalamus, diencephalon, optic tectum, midbrain tegmentum and rhombencephalon. Interestingly, numerous small pallial neurons express PSST1 and PSST6, although in different populations judging from the colocalization of TH immunoreactivity and PSST6 expression but not with PSST1. We observed expression of PSST1 in cerebrospinal fluid-contacting (CSF-c) neurons of the hypothalamic paraventricular organ and the central canal of the spinal cord. Unlike PSST1 and PSST6, PSST2 and PSST3 are only expressed in cells of the hypothalamus and in some hindbrain lateral reticular neurons, and PSST5 in cells of the region of the entopeduncular nucleus. Comparative data of brain expression of PSST genes indicates that the somatostatinergic system of sharks is the most complex reported in any fish. This article is protected by copyright. All rights reserved.
... The optic tectum in S. microcephalus and S. pacificus is notably reduced, and occupies ~2.5% of the brain; this relative reduction in tectum size is characteristic for deep-sea dwelling somniosids (Fig. 4H). The superficial layers of the optic tectum receive the majority of primary projections arising from the retinal ganglion cells and are associated with visual processing [125][126][127] , in addition to receiving projections from other sensory modalities 128 . Despite its role as a multimodal integration center, variability in the size of the optic tectum is suggested to reflect visual specialization in non-mammalian species 8,69,88 and often scales with a number of other aspects of the peripheral nervous system in fishes, including eye size, retinal area, the number of retinal ganglion cells and optic nerve axons, and overall retinal area 88,129,130 . ...
In cartilaginous fishes, variability in the size of the brain and its major regions is often associated with primary habitat and/or specific behavior patterns, which may allow for predictions on the relative importance of different sensory modalities. The Greenland (Somniosus microcephalus) and Pacific sleeper (S. pacificus) sharks are the only non-lamnid shark species found in the Arctic and are among the longest living vertebrates ever described. Despite a presumed visual impairment caused by the regular presence of parasitic ocular lesions, coupled with the fact that locomotory muscle power is often depressed at cold temperatures, these sharks remain capable of capturing active prey, including pinnipeds. Using magnetic resonance imaging (MRI), brain organization of S. microcephalus and S. pacificus was assessed in the context of up to 117 other cartilaginous fish species, using phylogenetic comparative techniques. Notably, the region of the brain responsible for motor control (cerebellum) is small and lacking foliation, a characteristic not yet described for any other large-bodied (>3 m) shark. Further, the development of the optic tectum is relatively reduced, while olfactory brain regions are among the largest of any shark species described to date, suggestive of an olfactory-mediated rather than a visually-mediated lifestyle.
... Moreover, the suprachiasmatic nucleus expressed melatonin receptors in sea bass (Herrera-Pérez et al. 2010) and the presence of abundant melatonin binding sites was reported in the preoptic area of different teleost species (Martinoli et al. 1991, Ekström and Vanĕcek 1992, Mazurais et al. 1999, Herrera-Pérez et al. 2010). This nucleus is also known as a retinorecipient area in fish (Fernald 1982, Presson et al. 1985, Repérant et al. 1986, Medina et al. 1990, Northcutt and Butler 1993. In Senegalese sole, retinofugal projections and retinopetal neurons were also found at the level of the suprachiasmatic area (Confente 2009), suggesting that this nucleus could play a relevant role in the transduction of light information from both photoreceptor centres. ...
... A small number of axons also project to ipsilateral visual centres. 171,173 The retinal ganglion cells project to the tectum in a strict retinotopic spatial order, with retinal specialisations such as a visual streak being over-represented. 174,175 As the tectum is the primary projection site for the majority of retinal ganglion cell axons in sharks and, as in bony fishes, tends to be well developed in species with large eyes, 172 the relative size of this structure may be an indicator of the relative importance of vision, when comparing this measure with relative brain size (encephalisation). ...
The eyes of apex predators, such as the shark, have fascinated comparative visual neuroscientists for hundreds of years with respect to how they perceive the dark depths of their ocean realm or the visual scene in search of prey. As the earliest representatives of the first stage in the evolution of jawed vertebrates, sharks have an important role to play in our understanding of the evolution of the vertebrate eye, including that of humans. This comprehensive review covers the structure and function of all the major ocular components in sharks and how they are adapted to a range of underwater light environments. A comparative approach is used to identify: species‐specific diversity in the perception of clear optical images; photoreception for various visual behaviours; the trade‐off between image resolution and sensitivity; and visual processing under a range of levels of illumination. The application of this knowledge is also discussed with respect to the conservation of this important group of cartilaginous fishes.
... There are no specific studies of the connections of the pretectum in non-teleost bony fishes and elasmobranches, which exhibit a less differentiated pretectal nuclear organization than teleosts although superficial, central and periventricular nuclei/regions have been recognized (Northcutt, 1979;Northcutt & Wathey, 1980;Rep erant et al., 1986;Rupp & Northcutt, 1998). The absence of specific connectional studies in these fishes precludes any detailed comparison with the various pretectal nuclei of zebrafish and other teleosts. ...
... The absence of specific connectional studies in these fishes precludes any detailed comparison with the various pretectal nuclei of zebrafish and other teleosts. However, experimental studies have revealed that the pretectum receives afferents from the retina and the pineal (elasmobranches: Northcutt, 1979;Northcutt & Wathey, 1980;Smeets, 1981a;Rep erant et al., 1986;Mandado, Huesa et al., 2003), and has reciprocal connections with the optic tectum (elasmobranches: Smeets, 1981bSmeets, ,1982sturgeon: Yamamoto, Yoshimoto, Albert, Sawai, & Ito, 1999). In sturgeon, the pretectum also receives scarce fibers from the telencephalon (Huesa, Anad on, & Y añez, 2006). ...
The pretectum is a complex region of the caudal diencephalon which in adult zebrafish comprises both retinorecipient (parvocellular superficial, central, intercalated, paracommissural and periventricular) and non-retinorecipient (magnocellular superficial, posterior and accessory) pretectal nuclei distributed from periventricular to superficial regions. We conducted a comprehensive study of the connections of pretectal nuclei by using neuronal tracing with fluorescent carbocyanine dyes. This study reveals specialization of efferent connections of the various pretectal nuclei, with nuclei projecting to the optic tectum (paracommissural, central and periventricular pretectal nuclei), the torus longitudinalis and the cerebellar corpus (paracommissural, central and intercalated pretectal nuclei), the lateral hypothalamus (magnocellular superficial, posterior and central pretectal nuclei), and the tegmental regions (accessory and superficial pretectal nuclei). With regard to major central afferents to the pretectum, we observed projections from the telencephalon to the paracommissural and central pretectal nuclei, from the optic tectum to the paracommissural, central, accessory and parvocellular superficial pretectal nuclei, from the cerebellum to the paracommissural and periventricular pretectal nuclei and from the nucleus isthmi to the parvocellular superficial and accessory pretectal nuclei. The parvocellular superficial pretectal nucleus sends conspicuous projections to the contralateral magnocellular superficial pretectal nucleus. The composite figure of results reveals large differences in connections of neighbor pretectal nuclei, indicating high degree of nuclear specialization. Our results will have important bearings in functional studies that analyze the relationship between specific circuits and behaviors in zebrafish. Comparison with results available in other species also reveals differences in the organization and connections of the pretectum in vertebrates. This article is protected by copyright. All rights reserved.
... The alar plate of the midbrain gives rise to the optic tectum, a layered structure containing at least five strata (Smeets et al., 1983;Anadón, 1991a,b, 1993), with the outer layers being the main recipient of visual inputs (Northcutt, 1979;Repérant et al., 1986), while the deep tectal layers receive nonvisual information. The outer cell layer contains abundant glycinergic cells (Anadón et al., 2013) and cells containing calcitonin genee related peptide (CGRP) (Molist et al., 1995), a neuromodulator in cholinergic and some noncholinergic pathways. ...
In this chapter we present a modern interpretation of the regional organization of the chondrichthyan brain mainly based on updated genoarchitectonic, neurochemical, and, in a lesser extent, hodological data in the brain of the catshark Scyliorhinus canicula . Particularly, the comparative analysis of the spatiotemporal expression patterns of developmental genes using this shark species as representative of basal gnathostomes has proved to be essential for recognizing the functional regionalization of the chondrichthyan brain, identifying common and divergent patterns in the specification of brain subdivisions, and, eventually, better understanding the diversity of vertebrate nervous systems.
... As in other vertebrates, the optic tectum (analogous to the superior colliculus in mammals) consists of paired lobes that form the roof of the mesencephalon (Barton et al., 1995). This region is comprised of alternating fiber and cellular layers, although debate persists concerning the number of tectal layers in cartilaginous fishes and the extent to which this characteristic varies intra-and interspecifically (Farner, 1978;Northcutt, 1979;Smeets, 1981;Ebbesson, 1984;Reperant et al., 1986;Manso and Anadon, 1991). The optic tectum is most readily associated with vision and visual processing, as it receives its major input from retinofugal fibers arising from the RGCs (Graeber and Ebbesson, 1972a,b;Northcutt, 1978Northcutt, , 1979Reperant et al., 1986;Hofmann, 1999). ...
... This region is comprised of alternating fiber and cellular layers, although debate persists concerning the number of tectal layers in cartilaginous fishes and the extent to which this characteristic varies intra-and interspecifically (Farner, 1978;Northcutt, 1979;Smeets, 1981;Ebbesson, 1984;Reperant et al., 1986;Manso and Anadon, 1991). The optic tectum is most readily associated with vision and visual processing, as it receives its major input from retinofugal fibers arising from the RGCs (Graeber and Ebbesson, 1972a,b;Northcutt, 1978Northcutt, , 1979Reperant et al., 1986;Hofmann, 1999). These projections are organized topographically; that is, the optic tectum contains a map of an animal's visual space (Bodznick, 1991). ...
1. Introduction2. The Visual System 2.1. The Eye and Image Formation2.2. Photoreception and Spectral Sensitivity2.3. The Retina and the Choroidal Tapetum2.4. Visual Sampling2.5. Visual Abilities3. The Non-visual System4. The Auditory and Vestibular Systems 4.1. The Inner Ear4.2. Vestibular Control4.3. Auditory Abilities5. The Electrosensory System 5.1. Structure and Spatial Sampling of the Ampullary Organs5.2. Role in Passive Electroreception5.3. Role in Magnetoreception6. The Lateral Line System 6.1. Canal and Superficial Neuromasts6.2. Sensitivity to Hydrodynamic Stimuli7. Cutaneous Mechanoreception8. The Chemosensory Systems 8.1. The Olfactory Apparatus and the Sampling of Water-Borne Substances8.2. Olfactory Sensitivity8.3. The Gustatory Apparatus8.4. Gustatory Sampling and Sensitivity8.5. The Common Chemical Sense9. Sensory Input to the Central Nervous System in Elasmobranchs 9.1. Neuroanatomy9.2. Assessing the Relative Importance of Each Sensory Modality9.3. Encephalization9.4. Neuroecology10. Perspectives on Future DirectionsElasmobranchs occupy a diversity of ecological niches with each species adapted to a complex set of environmental conditions. These conditions can be defined as a web of environmental signals, which are detected by a battery of senses, that have enabled these apex predators to survive relatively unchanged for over 400 million years. Signals such as light, odors, electric and magnetic fields, sound, and hydrodynamic disturbances all form a sensoryscape that each species can detect and process. However, the biophysical signals and their propagation within each ecological niche differ and place selection pressures on the ability of a specific sensory modality to detect and respond to prey, predator, and mate. This review investigates how elasmobranchs sense their environment by examining a diversity of species from different habitats, the ways in which they sample their sensoryscape, the sensitivity of each of their senses, and the effect this has on their behavior. The relative importance of each sensory modality is also investigated and how sensory input to the central nervous system can be assessed and used as a predictor of behavior. Although there is still a great deal we do not understand about elasmobranch sensory systems, the anatomical, physiological, molecular, and bioimaging approaches currently being used are enabling us to ask complex behavioral questions of these impressive predators.
... Also in reptiles, displaced GCs have been found to send fibers to the accessory optic system [eastern painted turtle, Chemisemys picta picta: and red-eared slider turtle, Trachemys (Pseudemys) scripta elegans: Reiner, 1981; veiled chameleon, Chamaeleo calyptratus: Bellintani-Guardia and Ott, 2002]. Although it is known that in elasmobranchs the retina projects to a tegmental region (presumed accessory optic nucleus) [Smeets, 1981;Repérant et al., 1986;Northcutt, 1991], the morphology or type of GCs that project to the tegmental region in question remains unknown. In the present study, both types of large GCs (IV and V) contained subtypes of GCs (type IV-1, type V-1, and type V-2) with their somas in the INL. ...
Retinal ganglion cells (GCs) in the Japanese catshark Scyliorhinus torazame were labeled retrogradely with biotinylated dextran amine (BDA3000). First the labeled cells were classified into 5 morphological types (types I-III: small GCs; types IV and V: large GCs) according to the size of the soma and the dendritic arborization pattern as seen in retinal wholemounts. Type I cells were stellate, with dendrites radiating in different directions. Type II cells had bipolar dendritic trees, with 2 primary dendrites extending in opposite directions. Type III cells had a single thick primary dendrite. Type IV cells were stellate, with dendrites covering a large area centered on the cell body. Type V cells were asymmetric, with most dendrites extending opposite to the axon as a large, fan-shaped dendritic field. Subsequently a wholemount was cross-sectioned, and we classified cells further into multiple subtypes according to the level of dendritic arborization within the inner plexiform layer. The present results suggest the existence of many types of GCs in elasmobranchs in addition to the 3 types of large GCs that have been characterized previously. Some of the newly described GC subtypes in the catshark retina appear to be similar to some of those reported in actinopterygians. © 2014 S. Karger AG, Basel.
