An immunohistochemical study of the telencephalon of the african lungfish, Protopterus annectens

Anton Reiner, R. Glenn Northcutt

Research output: Contribution to journalArticle

126 Citations (Scopus)

Abstract

The telencephalon of the African lungflsh, Protopterus annectens, was studied by immunohistochemical techniques in order to identify the major subdivisions of the telencephalon and determine the possible homologues of these subdivisions, if any, in other vertebrates. The distributions of four different neuropeptides (substance P, leucine‐enkephalin, avian pancreatic polypeptide, and LANT6), a neurotransmitter (serotonin), and a neurotransmitter‐related enzyme that is involved in catecholamine synthesis (tyrosine hydroxylase) were examined. The resultant labeling patterns indicated that the telencephalon of lungfish consists of three major subdivisions–a rostrally and dorsally situated olfactory bulb, a dorsally situated pallial region located caudal to the olfactory bulbs, and a ventrally situated subpallial regions. The dorsal and lateral pallial regions, which both receive secondary olfactory input, are somewhat, distinct from one another cytoarchitectonically, but their immunohistochemical, labeling characteristics did not differ. Thus, the lateral pallium and the dorsal pallium together appear to constitute an olfactory pallium in lungfishes. The medial pallium was found to consist of three immunohisthochemically distinct subdivisions–a dorsal cell group, an intermediate cell group, and a ventral cell group. These medial pallial fields extend throughout the entire rostrocaudal extent of the medial wall of the telencephalon. Although one or more of these medial pallial cell groups may be homologous to specific portions of the medial pallium in land vertebrates, no specific similarities were observed to support any proposed one‐to‐one correspondences. The possibility that one or more of the medial pallial cell groups of lungfishes correspond to cell groups located in the dorsal pallium of land vertebrates could not be excluded. The subpallium is divided into lateral, medial, and caudal subdivisions. The lateral subdivision appears to be homologous to the basal ganglia of land vertebrates since it contains neuropeptide/neurotransmitter‐specific neuronal populations that are characterstic of the striatal and pallidal portions of the basal ganglia of amniotes. The medial subdivision of the subpallium shows the topographic and immunohistochemical characteristics of the septal region and the nucleus accumbens region of the amniote telencephalon. The caudal subpallium does not show any distinctive immunohistochemical labeling characteristics and its possible homologue in land vertebrates is unclear. The present results indicate that the evolution of the telencephalon during the transition from fish to amphibians must have been characterized by a striking conservatism in the case of the subpallium. A basal ganglia and a septal region having many of the characteristics of those of land vertebrates appear to be present in the telencephalon of lungfishes, thereby suggesting that these cell groups were already present in the brains of the earliest lobe‐finned fishes. Although the present results suggest that a lateral pallium, or olfactory cortex, was present in the telencephalon of ancestral lobe‐finned fish, they do not provide evidence to support the existence in lobe‐finned fish of a forerunner of the dorsal pallium of land vertebrates. Further, it is unclear whether the medial pallial cell groups in lungfishes are homologous to cell groups in the medial telencephalic walls of land vertebrates.

Original languageEnglish (US)
Pages (from-to)463-481
Number of pages19
JournalJournal of Comparative Neurology
Volume256
Issue number3
DOIs
StatePublished - Jan 1 1987

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Telencephalon
Vertebrates
Fishes
Basal Ganglia
Septum of Brain
Olfactory Bulb
Neuropeptides
Corpus Striatum
Septal Nuclei
Nucleus Accumbens
Tyrosine 3-Monooxygenase
Amphibians
Politics
Substance P
Catecholamines
Neurotransmitter Agents
Serotonin

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

An immunohistochemical study of the telencephalon of the african lungfish, Protopterus annectens. / Reiner, Anton; Northcutt, R. Glenn.

In: Journal of Comparative Neurology, Vol. 256, No. 3, 01.01.1987, p. 463-481.

Research output: Contribution to journalArticle

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AB - The telencephalon of the African lungflsh, Protopterus annectens, was studied by immunohistochemical techniques in order to identify the major subdivisions of the telencephalon and determine the possible homologues of these subdivisions, if any, in other vertebrates. The distributions of four different neuropeptides (substance P, leucine‐enkephalin, avian pancreatic polypeptide, and LANT6), a neurotransmitter (serotonin), and a neurotransmitter‐related enzyme that is involved in catecholamine synthesis (tyrosine hydroxylase) were examined. The resultant labeling patterns indicated that the telencephalon of lungfish consists of three major subdivisions–a rostrally and dorsally situated olfactory bulb, a dorsally situated pallial region located caudal to the olfactory bulbs, and a ventrally situated subpallial regions. The dorsal and lateral pallial regions, which both receive secondary olfactory input, are somewhat, distinct from one another cytoarchitectonically, but their immunohistochemical, labeling characteristics did not differ. Thus, the lateral pallium and the dorsal pallium together appear to constitute an olfactory pallium in lungfishes. The medial pallium was found to consist of three immunohisthochemically distinct subdivisions–a dorsal cell group, an intermediate cell group, and a ventral cell group. These medial pallial fields extend throughout the entire rostrocaudal extent of the medial wall of the telencephalon. Although one or more of these medial pallial cell groups may be homologous to specific portions of the medial pallium in land vertebrates, no specific similarities were observed to support any proposed one‐to‐one correspondences. The possibility that one or more of the medial pallial cell groups of lungfishes correspond to cell groups located in the dorsal pallium of land vertebrates could not be excluded. The subpallium is divided into lateral, medial, and caudal subdivisions. The lateral subdivision appears to be homologous to the basal ganglia of land vertebrates since it contains neuropeptide/neurotransmitter‐specific neuronal populations that are characterstic of the striatal and pallidal portions of the basal ganglia of amniotes. The medial subdivision of the subpallium shows the topographic and immunohistochemical characteristics of the septal region and the nucleus accumbens region of the amniote telencephalon. The caudal subpallium does not show any distinctive immunohistochemical labeling characteristics and its possible homologue in land vertebrates is unclear. The present results indicate that the evolution of the telencephalon during the transition from fish to amphibians must have been characterized by a striking conservatism in the case of the subpallium. A basal ganglia and a septal region having many of the characteristics of those of land vertebrates appear to be present in the telencephalon of lungfishes, thereby suggesting that these cell groups were already present in the brains of the earliest lobe‐finned fishes. Although the present results suggest that a lateral pallium, or olfactory cortex, was present in the telencephalon of ancestral lobe‐finned fish, they do not provide evidence to support the existence in lobe‐finned fish of a forerunner of the dorsal pallium of land vertebrates. Further, it is unclear whether the medial pallial cell groups in lungfishes are homologous to cell groups in the medial telencephalic walls of land vertebrates.

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