The Conservative Evolution of the Vertebrate Basal Ganglia

Reiner, Anton

doi:10.1016/b978-0-12-802206-1.00004-0

Cited by 13 publications

(16 citation statements)

References 467 publications

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“…Dopaminergic innervation of BG nuclei is conserved across evolution, but the location and development of dopaminergic cell groups that project to these nuclei differ between anamniotes and amniotes (Reiner, 2016). TH is the rate-limiting enzyme for catecholamine biosynthesis and serves as a marker for dopaminergic and noradrenergic neurons (Molinoff & Axelrod, 1971).…”

Section: Discussionmentioning

confidence: 99%

“…Through the course of evolution, the expansion of both the pallium and subpallium caused several changes to occur in the BG organization to accommodate for the increasing number of telencephalic neurons. Tegmental DA input into the striatum became more substantial and motor control occurred via pallial motor areas rather than directly to the pretectal region (Reiner, 2016). In mammals, the evolution from a simple pallium to a multilayered neocortex led to the BG occupying a more central position within the telencephalon due to extensive lateroventral migration from pallial neurons (Karten, 1969).…”

Section: Introductionmentioning

confidence: 99%

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Identification of Subpallial Neuronal Populations Across Zebrafish Larval Stages that Express Molecular Markers for the Striatum

Aguda

2021

Preprint

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Striatal neurons within the basal ganglia play a central role in vertebrate action selection; however, their location in larval zebrafish is not well defined. We assayed for conserved striatal markers in the zebrafish subpallium using fluorescent in situ hybridization (FISH) and immunohistochemistry. Whole mount FISH revealed an inhibitory neuronal cluster rostral to the anterior commissure that expresses tac1, the gene that encodes the precursor peptide for substance P. This molecular profile is shared by mammalian striatal direct pathway neurons. A second partially overlapping population of inhibitory neurons was identified that expresses penka, the gene that encodes the precursor peptide for enkephalin. This molecular profile is shared by striatal indirect pathway neurons. Immunostaining for substance P and enkephalin confirmed the presence of these peptides in the subpallium as well as the presence of dopaminergic innervation. The tac1 and penka populations were both found to increase linearly across larval stages. Together, these findings support the existence of a striatal homologue in larval zebrafish that grows to match the development and increasing behavioural complexity of the organism.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Identification of Subpallial Neuronal Populations Across Zebrafish Larval Stages that Express Molecular Markers for the Striatum

Aguda

2021

Preprint

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“…(2012, 2013). A recent transcriptomic analysis of mouse entopeduncular neurons and their connections (Wallace et al., 2017) as well as a review of the evolution of basal ganglia in mammals and other vertebrates (Reiner, 2016) followed the traditional homology assumption in spite of presenting contrary hodological and comparative evidence, respectively, no doubt influenced by the accumulated authority of the widespread literature opinions.…”

Section: Introductionmentioning

confidence: 99%

“…This analysis applies equally to other mammals and tetrapods in general (birds; reptiles; amphibia; Reiner, 2016; Reiner et al., 1998, 2004, 2005), as well as to gnathostome fishes, where a molecularly comparable primarily telencephalic pallidal anlage exists, even in cases where a ventricular bulge of the pallidal progenitor domain is absent (Cobos, Puelles, et al., 2001; Cobos, Shimamura, et al., 2001; Marin et al., 1997; Medina et al., 2014; Métin et al., 2007; Moreno et al., 2010, 2018; Moreno, Domínguez, et al., 2008; Moreno, González, et al., 2008; Moreno, Rétaux, et al., 2008; Puelles et al., 2000; Smeets et al., 2000). Recently, agnathans are thought to have also a telencephalic pallidal primordium and correlative pallido‐pallial migrations (Grillner & Robertson, 2016; Martínez‐de‐la‐Torre et al., 2011; Pombal et al., 2009; Stephenson‐Jones et al., 2011; Ericsson et al, 2012; Villar‐Cervino et al., 2008; Sugahara et al., 2022).…”

Section: Introductionmentioning

confidence: 99%

“…However, Paxinos and Watson (2014; their figures 43-46) exceptionally distinguish external and internal globus pallidus (GPE and GPI) components within the rodent telencephalic pallidum, admitting that the mouse EP is strictly a nonpallidal hypothalamic structure as argued by Puelles et al (2012Puelles et al ( , 2013. A recent transcriptomic analysis of mouse entopeduncular neurons and their connections (Wallace et al, 2017) as well as a review of the evolution of basal ganglia in mammals and other vertebrates (Reiner, 2016) followed the traditional homology assumption in spite of presenting contrary hodological and comparative evidence, respectively, no doubt influenced by the accumulated authority of the widespread literature opinions.…”

Section: Introductionmentioning

confidence: 99%

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Critical test of the assumption that the hypothalamic entopeduncular nucleus of rodents is homologous with the primate internal pallidum

Puelles,

Stühmer,

Rubenstein

et al. 2023

J of Comparative Neurology

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The globus pallidus (GP) of primates is divided conventionally into distinct internal and external parts. The literature repeats since 1930 the opinion that the homolog of the primate internal pallidum in rodents is the hypothalamic entopeduncular nucleus (embedded within fiber tracts of the cerebral peduncle). To test this idea, we explored its historic fundaments, checked the development and genoarchitecture of mouse entopeduncular and pallidal neurons, and examined relevant comparative connectivity data. We found that the extratelencephalic mouse entopeduncular structure consists of four different components arrayed along a dorsoventral sequence in the alar hypothalamus. The ventral entopeduncular nucleus (EPV), with GABAergic neurons expressing Dlx5&6 and Nkx2‐1, lies within the hypothalamic peduncular subparaventricular area. Three other formations—the dorsal entopeduncular nucleus (EPD), the prereticular entopeduncular nucleus (EPPRt), and the preeminential entopeduncular nucleus (EPPEm)—lie within the overlying paraventricular area, under the subpallium. EPD contains glutamatergic neurons expressing Tbr1, Otp, and Pax6. The EPPRt has GABAergic cells expressing Isl1 and Meis2, whereas the EPPEm population expresses Foxg1 and may be glutamatergic. Genoarchitectonic observations on relevant areas of the mouse pallidal/diagonal subpallium suggest that the GP of rodents is constituted as in primates by two adjacent but molecularly and hodologically differentiable telencephalic portions (both expressing Foxg1). These and other reported data oppose the notion that the rodent extratelencephalic entopeduncular nucleus is homologous to the primate internal pallidum. We suggest instead that all mammals, including rodents, have dual subpallial GP components, whereas primates probably also have a comparable set of hypothalamic entopeduncular nuclei. Remarkably, there is close similarity in some gene expression properties of the telencephalic internal GP and the hypothalamic EPV. This apparently underlies their notable functional analogy, sharing GABAergic neurons and thalamopetal connectivity.

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Organization of the catecholaminergic systems in the brain of lungfishes, the closest living relatives of terrestrial vertebrates

López

González

2017

J of Comparative Neurology

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Lungfishes are a group of sarcopterygian fishes currently considered the closest living relatives of tetrapods, and represent an interesting group for the study of evolutionary traits in the transition from fishes to tetrapods. Catecholaminergic systems in the brain are among the most carefully analyzed neurotransmitter systems in the brain of most vertebrate groups. Their organization shows major shared characteristics, although traits particular to each vertebrate class have also been found, primarily between anamniotes and amniotes. Given the relevance of lungfishes in evolutionary terms, the present study provides the first comprehensive and detailed map of the catecholaminergic structures in the brain of two representative species of lungfishes, an African lungfish (Protopterus dolloi) and the Australian lungfish (Neoceratodus forsteri), as revealed by immunohistochemistry. Distinct groups of catecholaminergic cells were observed in the olfactory bulb, pallium, and preoptic area of the telencephalon, and the subpallium is devoid of these cells. Hypothalamic and diencephalic groups were detected and, in particular, the dopaminergic nucleus of the periventricular organ was evidenced with dopamine antibodies but not with anti-tyrosine hydroxylase. A well developed mesostriatal system was revealed formed by conspicuous groups of dopamine cells in the midbrain tegmentum and profuse innervation of the subpallium. Comparison of these results with those from other classes of vertebrates shows numerous common traits shared by most groups and also highlights particular features in lungfishes different from actinopterygian fishes that resemble those of amphibians and amniotes.

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The Conservative Evolution of the Vertebrate Basal Ganglia

Cited by 13 publications

References 467 publications

Identification of Subpallial Neuronal Populations Across Zebrafish Larval Stages that Express Molecular Markers for the Striatum

Identification of Subpallial Neuronal Populations Across Zebrafish Larval Stages that Express Molecular Markers for the Striatum

Critical test of the assumption that the hypothalamic entopeduncular nucleus of rodents is homologous with the primate internal pallidum

Organization of the catecholaminergic systems in the brain of lungfishes, the closest living relatives of terrestrial vertebrates

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