Nitric oxide synthase activity reveals an asymmetrical organization of the frog habenulae during development: A histochemical and cytoarchitectonic study from tadpoles to the matureRana esculenta, with notes on the pineal complex

Guglielmotti, Vittorio; Fiorino, L

doi:10.1002/(sici)1096-9861(19990830)411:3<441::aid-cne7>3.0.co;2-n

Cited by 27 publications

(15 citation statements)

References 46 publications

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“…The habenula of Neoceratodus , in the dorsalmost part of alar p2, is devoid of nitrergic cells, similarly to most species of amniotes studied with the exceptions of the chicken and pigeon (Atoji et al, ; Brüning, ). The presence of nitrergic cells in the habenula of teleosts and amphibians is more variable, and they have been described in goldfish (Giráldez‐Pérez et al, ) and some species of anuran and caecilian amphibians (González et al, ; Guglielmotti & Fiorino, ; Muñoz et al, ). In addition, heavily NADPH‐d reactive cells have been reported in the habenula of the larval lamprey (Schober, Malz, et al, ), and NOS‐ir habenular cells have also been observed in the cladistian and holostean fishes (López et al, ; López, Lozano, Morales, & González, ).…”

Section: Discussionmentioning

confidence: 99%

Pattern of nitrergic cells and fibers organization in the central nervous system of the Australian lungfish,Neoceratodus forsteri(Sarcopterygii: Dipnoi)

López

Morona

González

2019

J of Comparative Neurology

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The Australian lungfish Neoceratodus forsteri is the only extant species of the order Ceratodontiformes, which retained most of the primitive features of ancient lobe finned‐fishes. Lungfishes are the closest living relatives of land vertebrates and their study is important for deducing the neural traits that were conserved, modified, or lost with the transition from fishes to land vertebrates. We have investigated the nitrergic system with neural nitric oxide synthase (NOS) immunohistochemistry and NADPH‐diaphorase (NADPH‐d) histochemistry, which yielded almost identical results except for the primary olfactory projections and the terminal and preoptic nerve fibers labeled only for NADPH‐d. Combined immunohistochemistry was used for simultaneous detection of NOS with catecholaminergic, cholinergic, and serotonergic structures, aiming to establish accurately the localization of the nitrergic elements and to assess possible interactions between these neurotransmitter systems. The results demonstrated abundant nitrergic cells in the basal ganglia, amygdaloid complex, preoptic area, basal hypothalamus, mesencephalic tectum and tegmentum, laterodorsal tegmental nucleus, reticular formation, spinal cord, and retina. In addition, low numbers of nitrergic cells were observed in the olfactory bulb, all pallial divisions, lateral septum, suprachiasmatic nucleus, prethalamic and thalamic areas, posterior tubercle, pretectum, torus semicircularis, cerebellar nucleus, interpeduncular nucleus, the medial octavolateral nucleus, nucleus of the solitary tract, and the dorsal column nucleus. Colocalization of NOS and tyrosine hydroxylase was observed in numerous cells of the ventral tegmental area/substantia nigra complex. Comparison with other vertebrates, using a neuromeric analysis, reveals that the nitrergic system of Neoceratodus shares many neuroanatomical features with tetrapods and particularly with amphibians.

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Section: Discussionmentioning

confidence: 99%

Pattern of nitrergic cells and fibers organization in the central nervous system of the Australian lungfish,Neoceratodus forsteri(Sarcopterygii: Dipnoi)

López

Morona

González

2019

J of Comparative Neurology

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“…Intense NADPH‐d activity has been reported for the habenula of the larval lamprey (Schober et al, ), and for the teleost Carassius auratus the habenula housed a dorsally located nitrergic cell population (Giráldez‐Pérez et al, ) with a 30% colocalization with cholinergic cells (Giráldez‐Pérez et al, ). This trait presents high variability in amphibians, for which nitrergic cells have been described in the ventral habenula of Rana and Dermophis (Muñoz et al, ; González et al, ), but not in Xenopus , Hyla , Litoria , or Pleurodeles (Brüning and Mayer, ; González et al, ; López and González, ; Pinelli et al, ), and evidence of the nitrergic habenular asymmetry was found only in Rana esculenta (Guglielmotti and Fiorino, ). Nitrergic cells have not been reported for the habenula of reptiles or mammals, whereas for birds they have been described from the dorsolateral and ventromedial nuclei of the chicken (Brüning, ) and the lateral habenular nucleus of the pigeon (Atoji et al, ).…”

Section: Discussionmentioning

confidence: 99%

Organization of the nitrergic neuronal system in the primitive bony fishesPolypterus senegalusandErpetoichthys calabaricus(Actinopterygii: Cladistia)

López

Lozano

Morona

et al. 2015

J of Comparative Neurology

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Cladistians are a group of basal actinopterygian fishes that constitute a good model for studying primitive brain features, most likely present in the ancestral bony fishes. The analysis of the nitrergic neurons (with the enzyme nitric oxide synthase; NOS) has helped in understanding important aspects of brain organization in all vertebrates studied. We investigated the nitrergic system of two cladistian species by means of specific antibodies against NOS and NADPH-diaphorase (NADPH-d) histochemistry, which, with the exception of the primary olfactory and terminal nerve fibers, labeled only for NADPH-d, yielded identical results. Double immunohistochemistry was conducted for simultaneous detection of NOS with tyrosine hydroxylase, choline acetyltransferase, calbindin, calretinin, and serotonin, to establish accurately the localization of the nitrergic neurons and fibers and to assess possible interactions between these neuroactive substances. The pattern of distribution in both species showed only subtle differences in the density of labeled cells. Distinct groups of NOS-immunoreactive cells were observed in pallial and subpallial areas, paraventricular region, tuberal and retromammillary hypothalamic areas, posterior tubercle, prethalamic and thalamic areas, optic tectum, torus semicircularis, mesencephalic tegmentum, interpeduncular nucleus, superior and middle reticular nuclei, magnocellular vestibular nucleus, solitary tract nucleus, nucleus medianus magnocellularis, the spinal cord and amacrine cells in the retina. Large neurons in cranial nerve sensory ganglia were also labeled. The comparison of these results with those from other vertebrates, using a neuromeric analysis, reveals a conserved pattern of organization of the nitrergic system from this primitive fish group to amniotes, including mammals.

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“…The medial subnucleus can be further subdivided into medial and lateral components, on the basis of biochemical and subcellular properties. For example, only the more lateral region of the left medial habenula shows intense nitric oxide synthase activity (Guglielmotti and Fiorino, 1999). Evidence for habenular subnuclear specialization has also come from studies on cartilaginous and teleost fish.…”

Section: Leftover-related Gene Expression Defines Habenular Subdomainsmentioning

confidence: 99%

Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target

et al. 2005

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The zebrafish epithalamus, consisting of the pineal complex and flanking dorsal habenular nuclei, provides a valuable model for exploring how left-right differences could arise in the vertebrate brain. The parapineal lies to the left of the pineal and the left habenula is larger, has expanded dense neuropil, and distinct patterns of gene expression from the right habenula. Under the influence of Nodal signaling, positioning of the parapineal sets the direction of habenular asymmetry and thereby determines the left-right origin of habenular projections onto the midbrain target, the interpeduncular nucleus (IPN). In zebrafish with parapineal reversal, neurons from the left habenula project to a more limited ventral IPN region where right habenular axons would normally project. Conversely, efferents from the right habenula adopt a more extensive dorsoventral IPN projection pattern typical of left habenular neurons. Three members of the leftover-related KCTD (potassium channel tetramerization domain containing) gene family are expressed differently by the left and right habenula, in patterns that define asymmetric subnuclei. Molecular asymmetry extends to protein levels in habenular efferents, providing additional evidence that left and right axons terminate within different dorsoventral regions of the midbrain target. Laser-mediated ablation of the parapineal disrupts habenular asymmetry and consequently alters the dorsoventral distribution of innervating axons. The results demonstrate that laterality of the dorsal forebrain influences the formation of midbrain connections and their molecular properties.

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Nitric oxide synthase activity reveals an asymmetrical organization of the frog habenulae during development: A histochemical and cytoarchitectonic study from tadpoles to the matureRana esculenta, with notes on the pineal complex

Cited by 27 publications

References 46 publications

Pattern of nitrergic cells and fibers organization in the central nervous system of the Australian lungfish,Neoceratodus forsteri(Sarcopterygii: Dipnoi)

Pattern of nitrergic cells and fibers organization in the central nervous system of the Australian lungfish,Neoceratodus forsteri(Sarcopterygii: Dipnoi)

Organization of the nitrergic neuronal system in the primitive bony fishesPolypterus senegalusandErpetoichthys calabaricus(Actinopterygii: Cladistia)

Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target

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