Development of the electrosensory nervous system of Eigenmannia (gymnotiformes)

II. The electrosensory lateral line lobe, midbrain, and cerebellum

Michael Lannoo, H. A. Vischer, L. Maler

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

The somatotopically and functionally organized electrosensory system of gymnotiform teleosts provides a model for the study of the formation of ordered nerve connections. This paper describes the development of the major electrosensory nuclei within the hind- and midbrain. All three main electrosensory nuclei - the electrosensory lateral line lobe (ELL), dorsal torus semicircularis (torus), and tectum - grow by adding cells at their caudolateral borders. Toral and tectal germinal zones arise from lateral ventrical outpocketings that either completely or partially close by maturity. In the ELL before day 5 postspawning, germinal cells form from an initial periventricular germinal zone, then migrate to the caudolateral border of the hindbrain and begin dividing. The ELL grows from two main germinal zones, one for the medial segment, and one for the three lateral tuberous segments. Within each ELL germinal zone, newly formed cells arise from two areas: granular cells arise from a ventral subzone, pyramidal cells are generated more dorsally. Granular cells remain in situ, whereas pyramidal cells may migrate rostromedially. Cells begin differentiating as soon as they are formed. Spherical and pyramidal cells send ascending axons into the internal plexiform layer by day 14-18 and the ELL gradually begins to assume its mature laminar appearance. The ELL grows caudally, preceding the caudal lobe of the cerebellum, which will eventually lie over and fuse with it. Primary electrosensory afferents enter the ELL by day 6; incoming afferents form four fascicles within the ELL, suggesting the formation of separate ELL segments. Unlabelled projections between labelled fields from a single nerve branch filled with HRP on day 7 suggest that somatotopic order is already present at this early age. In the periphery, receptor addition is unordered, occurring along nerve branch pathways. Meanwhile the ELL adds cells in an orderly fashion at its caudolateral border. This suggests that primary afferents shift position caudally with growth to maintain their somatotopic relationships. Because all three central nuclei are in topographic register and grow by adding cells caudally, during growth ELL efferents to the torus and toral efferents to the tectum may utilize pssive mechanisms, such as fiber-fiber interactions, to guide axons.

Original languageEnglish (US)
Pages (from-to)37-58
Number of pages22
JournalJournal of Comparative Neurology
Volume294
Issue number1
StatePublished - 1990
Externally publishedYes

Fingerprint

Gymnotiformes
Mesencephalon
Cerebellum
Nervous System
Pyramidal Cells
Rhombencephalon
Axons
Growth

Keywords

  • axonal guidance
  • segmentation
  • sensory systems
  • shifting connections
  • somatotopic maps

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Development of the electrosensory nervous system of Eigenmannia (gymnotiformes): II. The electrosensory lateral line lobe, midbrain, and cerebellum",
abstract = "The somatotopically and functionally organized electrosensory system of gymnotiform teleosts provides a model for the study of the formation of ordered nerve connections. This paper describes the development of the major electrosensory nuclei within the hind- and midbrain. All three main electrosensory nuclei - the electrosensory lateral line lobe (ELL), dorsal torus semicircularis (torus), and tectum - grow by adding cells at their caudolateral borders. Toral and tectal germinal zones arise from lateral ventrical outpocketings that either completely or partially close by maturity. In the ELL before day 5 postspawning, germinal cells form from an initial periventricular germinal zone, then migrate to the caudolateral border of the hindbrain and begin dividing. The ELL grows from two main germinal zones, one for the medial segment, and one for the three lateral tuberous segments. Within each ELL germinal zone, newly formed cells arise from two areas: granular cells arise from a ventral subzone, pyramidal cells are generated more dorsally. Granular cells remain in situ, whereas pyramidal cells may migrate rostromedially. Cells begin differentiating as soon as they are formed. Spherical and pyramidal cells send ascending axons into the internal plexiform layer by day 14-18 and the ELL gradually begins to assume its mature laminar appearance. The ELL grows caudally, preceding the caudal lobe of the cerebellum, which will eventually lie over and fuse with it. Primary electrosensory afferents enter the ELL by day 6; incoming afferents form four fascicles within the ELL, suggesting the formation of separate ELL segments. Unlabelled projections between labelled fields from a single nerve branch filled with HRP on day 7 suggest that somatotopic order is already present at this early age. In the periphery, receptor addition is unordered, occurring along nerve branch pathways. Meanwhile the ELL adds cells in an orderly fashion at its caudolateral border. This suggests that primary afferents shift position caudally with growth to maintain their somatotopic relationships. Because all three central nuclei are in topographic register and grow by adding cells caudally, during growth ELL efferents to the torus and toral efferents to the tectum may utilize pssive mechanisms, such as fiber-fiber interactions, to guide axons.",
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