Immunohistochemical Localization of DARPP-32 in the Brain of Two Lungfishes: Further Assessment of Its Relationship with the Dopaminergic System

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Lungfishes are the closest living relatives of land vertebrates, and their neuroanatomical organization is particularly relevant for deducing the neural traits that have been conserved, modified, or lost with the transition from fishes to land vertebrates. The immunohistochemical localization of calbindin (CB) and calretinin (CR) provides a powerful method for discerning segregated neuronal populations, fiber tracts, and neuropils and is here applied to the brains of Neoceratodus and Protopterus, representing the two extant orders of lungfishes. The results showed abundant cells containing these proteins in pallial and subpallial telencephalic regions, with particular distinct distribution in the basal ganglia, amygdaloid complex, and septum. Similarly, the distribution of CB and CR containing cells supports the division of the hypothalamus of lungfishes into neuromeric regions, as in tetrapods. The dense concentrations of CB and CR positive cells and fibers highlight the extent of the thalamus. As in other vertebrates, the optic tectum is characterized by numerous CB positive cells and fibers and smaller numbers of CR cells. The so-called cerebellar nucleus contains abundant CB and CR cells with long ascending axons, which raises the possibility that it could be homologized to the secondary gustatory nucleus of other vertebrates. The corpus of the cerebellum is devoid of CB and CR and cells positive for both proteins are found in the cerebellar auricles and the octavolateralis nuclei. Comparison with other vertebrates reveals that lungfishes share most of their features of calcium binding protein distribution with amphibians, particularly with salamanders.

Section: Discussionsupporting

confidence: 80%

“…The striatal and pallidal components of the basal ganglia in lungfishes have only been distinctly recognized with specific immunostaining (González & Northcutt, ; González et al, ; López, Morona, & González, ).…”

Section: Discussionmentioning

confidence: 99%

Regional chemoarchitecture of the brain of lungfishes based on calbindin D‐28K and calretinin immunohistochemistry

Morona

López

Northcutt

et al. 2018

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“…In the basal part of the midbrain, a conspicuous group of dopaminergic neurons has been demonstrated in Neoceratodus that was readily comparable to the ventral tegmental area/substantia nigra complex (VTA/SN; López & González, ), which shows reciprocal connections with the striatum as in amniotes (González et al, ; López, Morona, & González, ). This dopaminergic group is not present in actinopterygian fishes and is reduced in amphibians; therefore, the lungfish situation resembles more closely that of amniotes.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, the study of the neuroanatomy of lungfishes has experienced a new impulse with the application of immunohistochemical techniques that include the localization of neurotransmitters and other molecular markers, such as transcription factors and calcium binding proteins (see López, Morona, Moreno, & González, ; Morona et al, ). In particular, we have reported the organization of the cholinergic, serotonergic and catecholaminergic systems (López, Domínguez, Morona, Northcutt, & González, ; López & González, , ; López, Morona, & González, ) and these results allowed us to determine the extent to which this organization is comparable to that of tetrapods. In the present study, we extend our analysis to the nitrergic neuronal system in the brain of Neoceratodus forsteri .…”

Section: Introductionmentioning

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

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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.

“…These interneurons are scattered across all DT subdivisions in the alligator ( Figure 2d). The dorsal-most zone of the VT expresses PPP1R1B (DARPP32) and is likely the alligator striatum (Figure 2e, St) (L opez, Morona, & Gonz alez, 2017;Ouimet, LaMantia, Goldman-Rakic, Rakic, & Greengard, 1992;Reiner, Perera, Paullus, & Medina, 1998;Reiner et al, 2004).…”

Section: Orientation and Atlasmentioning

confidence: 99%

Molecular anatomy of the alligator dorsal telencephalon

Briscoe

Ragsdale

2018

The evolutionary relationships of the mammalian neocortex and avian dorsal telencephalon (DT) nuclei have been debated for more than a century. Despite their central importance to this debate, non-avian reptiles remain underexplored with modern molecular techniques. Reptile studies harbor great potential for understanding the changes in DT organization that occurred in the early evolution of amniotes. They may also help clarify the specializations in the avian DT, which comprises a massive, cell-dense dorsal ventricular ridge (DVR) and a nuclear dorsal-most structure, the Wulst. Crocodilians are phylogenetically and anatomically attractive for DT comparative studies: they are the closest living relatives of birds and have a strikingly bird-like DVR, but they also possess a highly differentiated reptile cerebral cortex. We studied the DT of the American alligator, Alligator mississippiensis, at late embryonic stages with a panel of molecular marker genes. Gene expression and cytoarchitectonic analyses identified clear homologs of all major avian DVR subdivisions including a mesopallium, an extensive nidopallium with primary sensory input territories, and an arcopallium. The alligator medial cortex is divided into three components that resemble the mammalian dentate gyrus, CA fields, and subiculum in gene expression and topography. The alligator dorsal cortex contains putative homologs of neocortical input, output, and intratelencephalic projection neurons and, most notably, these are organized into sublayers similar to mammalian neocortical layers. Our findings on the molecular anatomy of the crocodilian DT are summarized in an atlas of the alligator telencephalon.