Sexual experience influences mating-induced activity in nitric oxide synthase-containing neurons in the medial preoptic area

Nutsch, Victoria L.; Will, Ryan G.; Hattori, Tomoko; Tobiansky, Daniel J.; Domínguez, Juan M.

doi:10.1016/j.neulet.2014.07.021

Cited by 24 publications

(16 citation statements)

References 25 publications

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“…In the lungfish Protopterus dolloi, a NADPH‐d reactive cell group was also observed in the preoptic area (Northcutt, ), and similar separated preoptic subpopulations have been observed in cladistian and holostean fishes (López et al, ; López, Lozano, Morales, & González, ). Comparatively, the presence of nitrergic cells in the preoptic area is a primitive and conserved feature described in all anamniotes studied (Table ) and in birds (Atoji et al, ; Brüning, ; Cozzi et al, ), whereas it is present in some species of reptiles (Smeets et al, ) and mammals (Chachlaki, Garthwaite, & Prevot, ; Domínguez et al, ; Hadeishi & Wood, ; Nutsch et al, ; Reis et al, ). Functionally, NO in the preoptic region regulates sexual behavior (Nutsch et al, ).…”

Section: Discussionmentioning

confidence: 88%

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: 88%

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 preoptic area of the cladistians contains a small population of nitrergic cells in its rostral portion. Similarly, nitrergic preoptic cells have been identified in teleosts (Arévalo et al, ; Brüning et al, ; Anken and Rahmann, ; Ando et al, ; Giráldez‐Pérez et al, ; Gaikwad et al, ), lungfish (Northcutt, ), amphibians (Brüning and Mayer, ; González et al, , ; Muñoz et al, ; Lázár and Losonczy, ; Huynh and Boyd, ; Pinelli et al, ), reptiles (Smeets et al, ) with the exception of snake (Jiang and Terashima, ), birds (Brüning, ; Cozzi et al, ; Atoji et al, ), and some species of mammals (Hadeishi and Wood, ; Dominguez et al, ; Nutsch et al, ). Therefore, this trait seems to be conserved, especially in anamniotes, and reduced and variable in mammals, where the functional role of NO in the sexual behavior has been studied in the medial preoptic nucleus of rat (Nutsch 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 preoptic area of gars houses a remarkable population of nitrergic cells distinct from the TH-ir, ChAT-ir, and CB-ir populations also observed in this region. The presence of nitrergic cells in the preoptic area is a highly conserved feature observed in all anamniotes studied (Table 2), whereas it is a more variable feature in amniotes, being present in birds [Brüning, 1993;Cozzi et al, 1997;Atoji et al, 2001] and some species of reptiles and mammals [Hadeishi and Wood, 1996;Domínguez et al, 2006;Nutsch et al, 2014], where the role of NO in sexual behavior has been demonstrated [Nutsch et al, 2014]. It should be noted that gene expression data have highlighted that the preoptic area does not belong to the hypothalamus but it is part of the subpallial telencephalic territory [see Moreno and González, 2011;Domínguez et al, 2015] that is topologically adjacent to the dorsal hypothalamic territory, and similar observations have been obtained for gars [González et al, 2014].…”

Section: Forebrainmentioning

confidence: 92%

Pattern of Nitrergic Neuronal System Organization in the Brain of Two Holostean Fishes (Actinopterygii: Ginglymodi)

et al. 2017

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The study of the nitrergic system, formed by the networks of neurons containing the enzyme nitric oxide synthase (NOS), has been extremely useful in unraveling neuroanatomical features of the organization of the central nervous system of vertebrates. Thus, data are available for representatives of most vertebrate classes and, in particular, several studies have detailed the organization of this system in teleosts. In contrast, no information is available regarding this neurotransmission system in the brains of holosteans, an early diverged and poorly understood group of actinopterygian fishes, currently considered a sister group of teleosts that contains only 8 species. The present study provides the first detailed information on the distribution of nitrergic cell bodies and fibers in 2 holostean species of the genus Lepisosteus, the spotted gar L. oculatus and the Florida gar L. platyrhincus. NOS immunohistochemistry and the NADPH diaphorase (NADPH-d) histochemical reaction were used, and both techniques yielded identical results, with the exception of the primary olfactory and terminal nerve fibers, which only labeled for NADPH-d exclusively in L. oculatus. Double immunohistochemistry was conducted for the simultaneous detection of NOS with tyrosine hydroxylase, choline acetyltransferase, calbindin, calretinin, and serotonin to accurately establish the localization of the nitrergic neurons and fibers in the brain of holosteans, the neuroanatomy of which has been mostly neglected, and to assess possible interactions between these neuroactive substances. Distinct groups of nitrergic cells were located in subpallial areas, the basal hypothalamus, posterior tubercle, optic tectum and mesencephalic tegmentum, reticular formation, solitary tract nucleus, spinal cord, and amacrine cells in the retina. In addition, low numbers of nitrergic cells were observed in the pallium, suprachiasmatic nucleus, prethalamic and thalamic areas, torus lateralis and torus semicircularis, cerebellar and laterodorsal tegmental nuclei, and the ventral octavolateral area. Comparison of these results with those from other classes of vertebrates, and including a segmental analysis to correlate cell populations, reveals that the pattern of the nitrergic system in holosteans is very close to that in ancestral actinopterygian fishes and highlights conserved and derived traits.

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Sexual experience influences mating-induced activity in nitric oxide synthase-containing neurons in the medial preoptic area

Cited by 24 publications

References 25 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)

Pattern of Nitrergic Neuronal System Organization in the Brain of Two Holostean Fishes (Actinopterygii: Ginglymodi)

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