Serotonin-immunoreactive structures in the central nervous system of the garfish Lepisosteus productus (Semionotiformes, Osteichthyes)

Chibá, Akira; Oka, Shunya

doi:10.1016/s0304-3940(98)01011-8

Cited by 20 publications

(28 citation statements)

References 15 publications

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“…4 Parent and Northcutt [1982], Chiba and Oka [1999]. The 5-HT-ir cell group localized most rostrally in the brain of cladistians is formed by CSF-contacting cells in the preoptic area.…”

Section: Forebrainmentioning

confidence: 99%

“…On the basis of its morphogenetic patterning, this area is currently considered a nonevaginated part of the telencephalon [Flames et al, 2007;García-López et al, 2009;Sánchez-Arrones et al, 2009;Moreno and González, 2011;Domínguez et al, 2013a], located topologically dorsal to the hypothalamus [Puelles and Rubenstein, 2003]. This telencephalic group represents an ancient and shared feature conserved in anamniotes but lost secondarily in garfish [holostean], some teleosts, and urodele amphibians [Corio et al, 1992;Clairambault et al, 1994;Chiba and Oka, 1999;Lillesaar, 2011], whereas serotonergic cells in the preoptic area are totally absent in amniotes ( table 1 ).…”

Section: Forebrainmentioning

confidence: 99%

“…This serotonergic cell population represents a feature conserved in all groups of fishes studied and is variably present in amphibians, reptiles, and birds, whereas mammals lack spinal 5-HT-ir cells [Sako et al, 1986b;Kiehn et al, 1992;Branchereau et al, 2000;Lillesaar, 2011;. These cells may provide substantial intrinsic innervation of the spinal cord [Wallen et al, 1989;Stuesse and Cruce, 1991;Adrio et al, 1999;Chiba and Oka, 1999;Brustein et al, 2003b;Barreiro-Iglesias et al, 2008;Carrera et al, 2008;Gabriel et al, 2009;Lillesaar, 2011], although part of the 5-HT-ir fibers may arise from the inferior raphe, such as in elasmobranches, lungfishes, and amphibians [Ritchie et al, 1984;Ronan and Northcutt, 1985;Tan and Miletic, 1990], or at more rostral hindbrain levels, such as in lampreys [Brodin et al, 1986;Barreiro-Iglesias et al, 2008]. This descending serotonergic projection and the local innervation may play important roles in the modulation of locomotion at spinal levels, as has been demonstrated in lampreys and zebrafish [Wallén et al, 1989;Brustein et al, 2003a;Gabriel et al, 2009].…”

Section: Spinal Cordmentioning

confidence: 99%

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Organization of the Serotonergic System in the Central Nervous System of Two Basal Actinopterygian Fishes: the Cladistians Polypterus senegalus and Erpetoichthys calabaricus

López¹,

González²

2014

Brain Behav Evol

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Cladistians (Polypteriformes) are currently considered basal to other living ray-finned fishes (actinopterygians), and their brain organization is therefore critical to providing information about the primitive neural characters that existed in the earliest ray-finned fishes. The organization of the serotonergic system in the brain has been carefully analyzed in most vertebrate groups, and in the present study we provide the first detailed information on the distribution of serotonergic cell bodies and fibers in the central nervous system of representative species of the two extant genera of cladistians, i.e. Polypterus senegalus and Erpetoichthys calabaricus, by means of immunohistochemistry against serotonin (5-HT). Distinct groups of immunoreactive cells were detected in the preoptic area, the hypothalamic paraventricular organ, the pineal organ, the pretectal region, the long column of the raphe in the rhombencephalic midline, the spinal cord, and amacrine cells in the inner nuclear layer of the retina. Fiber labeling was widely distributed in all main brain subdivisions but was more abundant in distinct pallial and subpallial areas, the preoptic area, the thalamus, the optic tectum, the tori semicircularis and lateralis, the rhombencephalic reticular formation, the nucleus of the solitary tract, and the dorsal aspect of the spinal cord. Our analysis makes it possible to establish which serotonergic structures characterized the earliest ray-finned fishes, and a comparison of these results with those from other classes of vertebrates, including a segmental analysis to correlate cell populations, reveals that most characteristics, such as the presence of serotonergic cells in the preoptic area and the basal hypothalamus, are preserved in all anamniotes. However, this system seems to be reduced in amniotes, mainly mammals, although important features are shared, such as the presence of serotonergic cells in the pineal organ, the retina, and the raphe nuclei.

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“…4 Parent and Northcutt [1982], Chiba and Oka [1999]. The 5-HT-ir cell group localized most rostrally in the brain of cladistians is formed by CSF-contacting cells in the preoptic area.…”

Section: Forebrainmentioning

confidence: 99%

Section: Forebrainmentioning

confidence: 99%

Section: Spinal Cordmentioning

confidence: 99%

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Organization of the Serotonergic System in the Central Nervous System of Two Basal Actinopterygian Fishes: the Cladistians Polypterus senegalus and Erpetoichthys calabaricus

López¹,

González²

2014

Brain Behav Evol

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“…In contrast to the extensive experimental data about the organization of the CNS of teleosts, there is little information concerning the brain of holosteans. In particular, there are limited hodological data related to the visual and the lateral line systems Butler, 1976, 1980;Song and Northcutt, 1991;Collin and Northcutt, 1995], and several mapping studies of the distribution of monoamines [Parent and Northcutt, 1982;Chiba and Oka, 1999] and diverse neuropeptides [Malz et al, 1999;Baker and Bird, 2002;Chiba, 2005]. In addition, in a previous study we described in detail the organization of the brain cholinergic system [Morona et al, 2013].…”

Section: Introductionmentioning

confidence: 99%

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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“…In particular, a few studies of holosteans have reported some hodological features, mainly related to the visual and lateral line systems Butler, 1976, 1980;McCormick, 1981;Butler and Northcutt, 1982], and there are some data on the chemical neuroanatomy of the brain in these fishes: catecholamines and serotonin [Parent and Northcutt, 1982;Chiba and Oka, 1999]; acetylcholinesterase [Northcutt and Butler, 1993]; FMRFamide [Malz et al, 1999]; melanin-concentrating hormone [Baker and Bird, 2002] and neuropeptide-Y [Chiba, 2005].…”

Section: Introductionmentioning

confidence: 99%

Comparative Analysis of the Organization of the Cholinergic System in the Brains of Two Holostean Fishes, the Florida Gar Lepisosteus platyrhincus and the Bowfin Amia calva

Morona¹,

López²,

Northcutt³

et al. 2013

Brain Behav Evol

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The cholinergic system in the brain has been widely studied in most vertebrate groups, but there is no information available about this neurotransmission system in the brains of holostean fishes, a primitive and poorly understood group of actinopterygian fishes. The present study provides the first detailed information on the distribution of cholinergic cell bodies and fibers in the central nervous system in two holostean species, the Florida gar, Lepisosteus platyrhincus, and the bowfin, Amia calva. Immmunohistochemistry against the enzyme choline acetyltransferase (ChAT) revealed distinct groups of ChAT-immunoreactive (ChAT-ir) cells in the habenula, isthmic nucleus, laterodorsal tegmental nucleus, octavolateral area, reticular formation, cranial nerve motor nuclei and the motor column of the spinal cord, all of which seem to be highly conserved among vertebrates. Some ChAT-ir cells were detected in the basal telencephalon that appear in actinopterygians for the first time in the evolution of this neurotransmission system, whereas the remarkable cholinergic population in the optic tectum is a peculiar characteristic, the presence of which varies throughout evolution, although it is present in all teleosts studied. Abundant cholinergic fibers were found in the pretectal region and optic tectum, where they probably modulate vision, and in the hypothalamus and the interpeduncular neuropil. Some interspecific differences were also observed, such as the presence of ChAT-ir cells in the supraoptoparaventricular band only in Lepisosteus and in in the nucleus subglomerulosus only in Amia. In addition, ChAT-ir fibers in the olfactory bulb were detected only in Amia. Comparison of these results with those from other classes of vertebrates, and a segmental analysis to correlate cell populations, reveal that the pattern of the cholinergic system in holosteans is very close to that in ancestral actinopterygian fishes, as recently described in the bichir (Cladistia), although an important evolutionary novelty in holosteans is the presence of cholinergic cells in the basal telencephalon.

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Serotonin-immunoreactive structures in the central nervous system of the garfish Lepisosteus productus (Semionotiformes, Osteichthyes)

Cited by 20 publications

References 15 publications

Organization of the Serotonergic System in the Central Nervous System of Two Basal Actinopterygian Fishes: the Cladistians <b><i>Polypterus senegalus</i></b> and <b><i>Erpetoichthys calabaricus</i></b>

Organization of the Serotonergic System in the Central Nervous System of Two Basal Actinopterygian Fishes: the Cladistians <b><i>Polypterus senegalus</i></b> and <b><i>Erpetoichthys calabaricus</i></b>

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

Comparative Analysis of the Organization of the Cholinergic System in the Brains of Two Holostean Fishes, the Florida Gar <b><i>Lepisosteus platyrhincus</i></b> and the Bowfin <b><i>Amia calva</i></b>

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