Interspecific variation in the projection of primary afferents onto the electrosensory lateral line lobe of weakly electric teleosts: Different solutions to the same mapping problem

Michael Lannoo, L. Maler

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

We demonstrate that preterminal axons composing the primary afferent projection onto the four somatotopically organized electrosensory lateral line lobe (ELL) segments in weakly electric gymnotiform teleosts course in fundamentally different directions in the most commonly studied species. Afferents enter the deep fiber layer (dfl) of the ELL and course in variable, but species-specific, directions within a horizontal plane before turning dorsally to terminate within the deep neuropil layer of the ELL (dnl). Among the species considered here, apteronotids exhibit the tightest projection pattern. Afferents enter the rostral ELL from the anterior lateral line nerve ganglion (ALLNG) in a nonsomatotopic fashion. As they course horizontally, these fibers undergo a rostrocaudal somatotopic sorting along the ventrolateral border of the dfl, then turn within a horizontal plane to course medially across the ELL segments. These medially coursing horizontal fibers are sorted: they form sublaminae according to the nerve branch containing their peripheral axon. Horizontal axons then turn dorsally, form fascicles, and terminate within the dnl. Within the dorsal fascicles, axons run directly into the dnl with little deviation, and their terminal fields exhibit no appreciable spread. In sternopygids, dfl horizontal fibers course in directions orthogonal to those in apteronotids. Fibers enter the rostral ELL and course medially across segments before turning caudally within segments. Unlike apteronotids, sternopygid horizontal fibers do not sort tightly by nerve branch. As horizontal axons turn dorsally they also form tight fascicles. But rather than terminating directly and without spreading, as in apteronotids, sternopygid fibers disperse from these fascicles and become sorted horizontally a second time prior to terminating in the dnl. Gymnotids show a third pattern: their primary afferents course into the rostral ELL without an obvious organization, they form no tight laminae of horizontal fibers and no fascicles of dorsal fibers. Unlike the other gymnotiforms examined, afferents coursing to the gymnotid MS can take one of two routes, ventrally through the dfl in the manner of all other gymnotiforms, or, uniquely, dorsally through the plexiform layer of the ELL (pl), which is typically the location of ELL efferents. These afferents then turn ventrally to terminate. Variations in axonal trajectories do not appear to reflect major functional differences in the processing of electrosensory information, but instead may reflect the phylogenetic relationships of the developmental processes involved in guiding axons. We propose a simple model for the development of these different trajectories based on the assumption that among species similar guidance cues are expressed at different times as the projection develops.

Original languageEnglish (US)
Pages (from-to)153-160
Number of pages8
JournalJournal of Comparative Neurology
Volume294
Issue number1
StatePublished - 1990
Externally publishedYes

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Axons
Neuropil
Gymnotiformes
Automatic Data Processing
Ganglia
Cues
Direction compound

Keywords

  • axonal trajectories
  • fasciculation
  • Gymnotiformes
  • sensory maps
  • somatotopic projections

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Interspecific variation in the projection of primary afferents onto the electrosensory lateral line lobe of weakly electric teleosts: Different solutions to the same mapping problem",
abstract = "We demonstrate that preterminal axons composing the primary afferent projection onto the four somatotopically organized electrosensory lateral line lobe (ELL) segments in weakly electric gymnotiform teleosts course in fundamentally different directions in the most commonly studied species. Afferents enter the deep fiber layer (dfl) of the ELL and course in variable, but species-specific, directions within a horizontal plane before turning dorsally to terminate within the deep neuropil layer of the ELL (dnl). Among the species considered here, apteronotids exhibit the tightest projection pattern. Afferents enter the rostral ELL from the anterior lateral line nerve ganglion (ALLNG) in a nonsomatotopic fashion. As they course horizontally, these fibers undergo a rostrocaudal somatotopic sorting along the ventrolateral border of the dfl, then turn within a horizontal plane to course medially across the ELL segments. These medially coursing horizontal fibers are sorted: they form sublaminae according to the nerve branch containing their peripheral axon. Horizontal axons then turn dorsally, form fascicles, and terminate within the dnl. Within the dorsal fascicles, axons run directly into the dnl with little deviation, and their terminal fields exhibit no appreciable spread. In sternopygids, dfl horizontal fibers course in directions orthogonal to those in apteronotids. Fibers enter the rostral ELL and course medially across segments before turning caudally within segments. Unlike apteronotids, sternopygid horizontal fibers do not sort tightly by nerve branch. As horizontal axons turn dorsally they also form tight fascicles. But rather than terminating directly and without spreading, as in apteronotids, sternopygid fibers disperse from these fascicles and become sorted horizontally a second time prior to terminating in the dnl. Gymnotids show a third pattern: their primary afferents course into the rostral ELL without an obvious organization, they form no tight laminae of horizontal fibers and no fascicles of dorsal fibers. Unlike the other gymnotiforms examined, afferents coursing to the gymnotid MS can take one of two routes, ventrally through the dfl in the manner of all other gymnotiforms, or, uniquely, dorsally through the plexiform layer of the ELL (pl), which is typically the location of ELL efferents. These afferents then turn ventrally to terminate. Variations in axonal trajectories do not appear to reflect major functional differences in the processing of electrosensory information, but instead may reflect the phylogenetic relationships of the developmental processes involved in guiding axons. We propose a simple model for the development of these different trajectories based on the assumption that among species similar guidance cues are expressed at different times as the projection develops.",
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T1 - Interspecific variation in the projection of primary afferents onto the electrosensory lateral line lobe of weakly electric teleosts

T2 - Different solutions to the same mapping problem

AU - Lannoo, Michael

AU - Maler, L.

PY - 1990

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N2 - We demonstrate that preterminal axons composing the primary afferent projection onto the four somatotopically organized electrosensory lateral line lobe (ELL) segments in weakly electric gymnotiform teleosts course in fundamentally different directions in the most commonly studied species. Afferents enter the deep fiber layer (dfl) of the ELL and course in variable, but species-specific, directions within a horizontal plane before turning dorsally to terminate within the deep neuropil layer of the ELL (dnl). Among the species considered here, apteronotids exhibit the tightest projection pattern. Afferents enter the rostral ELL from the anterior lateral line nerve ganglion (ALLNG) in a nonsomatotopic fashion. As they course horizontally, these fibers undergo a rostrocaudal somatotopic sorting along the ventrolateral border of the dfl, then turn within a horizontal plane to course medially across the ELL segments. These medially coursing horizontal fibers are sorted: they form sublaminae according to the nerve branch containing their peripheral axon. Horizontal axons then turn dorsally, form fascicles, and terminate within the dnl. Within the dorsal fascicles, axons run directly into the dnl with little deviation, and their terminal fields exhibit no appreciable spread. In sternopygids, dfl horizontal fibers course in directions orthogonal to those in apteronotids. Fibers enter the rostral ELL and course medially across segments before turning caudally within segments. Unlike apteronotids, sternopygid horizontal fibers do not sort tightly by nerve branch. As horizontal axons turn dorsally they also form tight fascicles. But rather than terminating directly and without spreading, as in apteronotids, sternopygid fibers disperse from these fascicles and become sorted horizontally a second time prior to terminating in the dnl. Gymnotids show a third pattern: their primary afferents course into the rostral ELL without an obvious organization, they form no tight laminae of horizontal fibers and no fascicles of dorsal fibers. Unlike the other gymnotiforms examined, afferents coursing to the gymnotid MS can take one of two routes, ventrally through the dfl in the manner of all other gymnotiforms, or, uniquely, dorsally through the plexiform layer of the ELL (pl), which is typically the location of ELL efferents. These afferents then turn ventrally to terminate. Variations in axonal trajectories do not appear to reflect major functional differences in the processing of electrosensory information, but instead may reflect the phylogenetic relationships of the developmental processes involved in guiding axons. We propose a simple model for the development of these different trajectories based on the assumption that among species similar guidance cues are expressed at different times as the projection develops.

AB - We demonstrate that preterminal axons composing the primary afferent projection onto the four somatotopically organized electrosensory lateral line lobe (ELL) segments in weakly electric gymnotiform teleosts course in fundamentally different directions in the most commonly studied species. Afferents enter the deep fiber layer (dfl) of the ELL and course in variable, but species-specific, directions within a horizontal plane before turning dorsally to terminate within the deep neuropil layer of the ELL (dnl). Among the species considered here, apteronotids exhibit the tightest projection pattern. Afferents enter the rostral ELL from the anterior lateral line nerve ganglion (ALLNG) in a nonsomatotopic fashion. As they course horizontally, these fibers undergo a rostrocaudal somatotopic sorting along the ventrolateral border of the dfl, then turn within a horizontal plane to course medially across the ELL segments. These medially coursing horizontal fibers are sorted: they form sublaminae according to the nerve branch containing their peripheral axon. Horizontal axons then turn dorsally, form fascicles, and terminate within the dnl. Within the dorsal fascicles, axons run directly into the dnl with little deviation, and their terminal fields exhibit no appreciable spread. In sternopygids, dfl horizontal fibers course in directions orthogonal to those in apteronotids. Fibers enter the rostral ELL and course medially across segments before turning caudally within segments. Unlike apteronotids, sternopygid horizontal fibers do not sort tightly by nerve branch. As horizontal axons turn dorsally they also form tight fascicles. But rather than terminating directly and without spreading, as in apteronotids, sternopygid fibers disperse from these fascicles and become sorted horizontally a second time prior to terminating in the dnl. Gymnotids show a third pattern: their primary afferents course into the rostral ELL without an obvious organization, they form no tight laminae of horizontal fibers and no fascicles of dorsal fibers. Unlike the other gymnotiforms examined, afferents coursing to the gymnotid MS can take one of two routes, ventrally through the dfl in the manner of all other gymnotiforms, or, uniquely, dorsally through the plexiform layer of the ELL (pl), which is typically the location of ELL efferents. These afferents then turn ventrally to terminate. Variations in axonal trajectories do not appear to reflect major functional differences in the processing of electrosensory information, but instead may reflect the phylogenetic relationships of the developmental processes involved in guiding axons. We propose a simple model for the development of these different trajectories based on the assumption that among species similar guidance cues are expressed at different times as the projection develops.

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