Telencephalo–habenulo–interpeduncular connections in the brain of the shark Chiloscyllium arabicum

Giuliani, Anna Maria; Minelli, Daniela; Quaglia, Antonio; Villani, L.

doi:10.1016/s0006-8993(01)03310-8

Cited by 11 publications

(17 citation statements)

References 23 publications

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“…However, as these cells are located very close to the habenula, we cannot rule out the possibility of non-specific labeling in our experiments. Despite this caveat, results in other species seem to support this connection, as potentially homologous nuclei were described in the dorsal thalamus of a shark (Giuliani et al, 2002 ) and a lizard (Díaz and Puelles, 1992 ).…”

Section: Discussionmentioning

confidence: 91%

Afferent Connectivity of the Zebrafish Habenulae

Turner

Hawkins

Yáñez

et al. 2016

Front. Neural Circuits

143

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The habenulae are bilateral nuclei located in the dorsal diencephalon that are conserved across vertebrates. Here we describe the main afferents to the habenulae in larval and adult zebrafish. We observe afferents from the subpallium, nucleus rostrolateralis, posterior tuberculum, posterior hypothalamic lobe, median raphe; we also see asymmetric afferents from olfactory bulb to the right habenula, and from the parapineal to the left habenula. In addition, we find afferents from a ventrolateral telencephalic nucleus that neurochemical and hodological data identify as the ventral entopeduncular nucleus (vENT), confirming and extending observations of Amo et al. (2014). Fate map and marker studies suggest that vENT originates from the diencephalic prethalamic eminence and extends into the lateral telencephalon from 48 to 120 hour post-fertilization (hpf). No afferents to the habenula were observed from the dorsal entopeduncular nucleus (dENT). Consequently, we confirm that the vENT (and not the dENT) should be considered as the entopeduncular nucleus “proper” in zebrafish. Furthermore, comparison with data in other vertebrates suggests that the vENT is a conserved basal ganglia nucleus, being homologous to the entopeduncular nucleus of mammals (internal segment of the globus pallidus of primates) by both embryonic origin and projections, as previously suggested by Amo et al. (2014).

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Section: Discussionmentioning

confidence: 91%

Afferent Connectivity of the Zebrafish Habenulae

Turner

Hawkins

Yáñez

et al. 2016

Front. Neural Circuits

143

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“…Similar projections were also observed in the thornback guitarfish (Platyrhinoidis) after injections in the lateral pallium. A projection to the habenula from several telencephalic areas was also described by Giuliani et al [2002] in the bamboo shark Chiloscyllium . The authors found also both direct and indirect (via the habenula) projections to the mesencephalic interpeduncular nucleus, thus confirming the existence of a stria medullaris -fasciculus retroflexus pathway in elasmobranchs, as in all other vertebrates examined.…”

Section: Olfactory Pathwaysmentioning

confidence: 74%

Forebrain Organization in Elasmobranchs

Hofmann

Northcutt

2012

Brain Behav Evol

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It has long been known that many elasmobranch fishes have relatively large brains. The telencephalon, in particular, has increased in size in several groups, and as a percent of total brain weight, it is as large as in some mammals. Little is known, however, about the organization, connections, and functions of the telencephalon in elasmobranchs. Early experimental studies indicated that olfaction does not dominate the telencephalon and that other sensory modalities are represented, particularly in the pallium. We have investigated the intrinsic and extrinsic connections of the telencephalon in two elasmobranch species: the thornback guitarfish, Platyrhinoidis triseriata, and the spiny dogfish, Squalus acanthias. Tracers were injected into various parts of the forebrain and olfactory pathways were found to be extensive and were seen to involve the pallium. Injections into various parts of the pallium revealed a major input from the area basalis, which receives secondary and tertiary olfactory fibers. Nonolfactory input from the diencephalon appeared relatively minor and seemed to converge with olfactory information in the dorsal pallium and area superficialis basalis. Major descending projections were seen to originate in the dorsal pallium and terminate in the hypothalamus and – in the case of Platyrhinoidis – massively in the lateral mesencephalic nucleus. Descending pathways appeared mainly crossed in Platyrhinoidis, but not in Squalus. Our data indicate that the concept of the dorsal pallium as a nonolfactory area in elasmobranchs must be reconsidered, and we suggest that many telencephalic centers, including the dorsal pallium, are involved in olfactory orientation.

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“…The present study provides evidence for the role of the habenula as an evolutionary conserved link between basal ganglia, limbic, and sensory systems. In lampreys, chondrichthyes, teleosts, amphibians, reptiles, and mammals, habenular afferents originate mostly from telencephalic, diencephalic, and mesencephalic areas [lampreys: Yáñez & Anadón, , Stephenson‐Jones, Floros, et al, ; chondrichthyes: Giuliani, Minelli, Quaglia, & Villani, ; teleosts: Villani et al, , Yáñez & Anadón, , Hendricks & Jesuthasan, , Turner et al, ; amphibians: Kemali et al, , present study; reptiles: Díaz & Puelles, ; mammals: Herkenham & Nauta, , McBride, , Parent, Gravel, & Boucher, ]. During phylogenetic development, direct sensory innervation was gradually replaced by numerous inputs from limbic structures, as demonstrated for lampreys (Stephenson‐Jones, Floros, et al, ), anuran amphibians (present study), and mammals (cf.…”

Section: Discussionmentioning

confidence: 99%

The habenula as an evolutionary conserved link between basal ganglia, limbic, and sensory systems—A phylogenetic comparison based on anuran amphibians

Freudenmacher

Twickel

Walkowiak

2019

J of Comparative Neurology

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Based on anatomical and functional data, the habenula—a phylogenetically old brain structure present in all vertebrates—takes part in the integration of limbic, sensory, and basal ganglia information to guide effective response strategies appropriate to environmental conditions. In the present study, we investigated the connections of the habenular nuclei of the oriental fire‐bellied toad, Bombina orientalis, and compared them with published data from lampreys, chondrichthyes, teleosts, reptiles, birds, and mammals. During phylogenetic development, the primordial habenula circuitry underwent various evolutionary adaptations and in the tetrapod line, the circuit complexity increased. The habenula circuitry of anuran amphibians, decedents of the first land‐living tetrapods, seem to exhibit a mix of ancient as well as modern features. The anuran medial and lateral habenula homologs receive differential input from the septum, nucleus of the diagonal band of Broca, preoptic area, hypothalamus, rostral pallium, nucleus accumbens, ventral pallidum, and bed nucleus of the stria terminalis. Additional input arises from a border region in the ventral prethalamus, here discussed as a putative homolog of the entopeduncular nucleus of rodents. The habenular subnuclei also differentially innervate the interpeduncular nucleus, raphe nuclei, substantia nigra pars compacta and ventral tegmental area homologs, superficial mamillary area, laterodorsal tegmental nucleus, locus coeruleus, inferior and superior colliculus homologs, hypothalamus, preoptic area, septum, nucleus of the diagonal band of Broca, and main olfactory bulb. It seems likely that the main connectivity between the habenula and the basal ganglia, limbic, and sensory systems was already present in the common tetrapod ancestor.

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Telencephalo–habenulo–interpeduncular connections in the brain of the shark Chiloscyllium arabicum

Cited by 11 publications

References 23 publications

Afferent Connectivity of the Zebrafish Habenulae

Afferent Connectivity of the Zebrafish Habenulae

Forebrain Organization in Elasmobranchs

The habenula as an evolutionary conserved link between basal ganglia, limbic, and sensory systems—A phylogenetic comparison based on anuran amphibians

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