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A common evolutionary origin for the ON- and OFF-edge motion detection pathways of the Drosophila visual system.

Shinomiya K, Takemura SY, Rivlin PK, Plaza SM, Scheffer LK, Meinertzhagen IA - Front Neural Circuits (2015)

Bottom Line: Yet T4 receives input in the second neuropil, or medulla (ME), and T5 in the third neuropil or lobula (LO).Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate ME and LO neuropils, and that a fiber crossing-the internal chiasma-arose between the two neuropils.The split most plausibly occurred, we suggest, with the formation of the LO as a new neuropil that formed when it separated from its ancestral neuropil to leave the ME, suggesting additionally that ME input neurons to T4 and T5 may also have had a common origin.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology and Neuroscience, Life Sciences Centre, Dalhousie University Halifax, NS, Canada ; FlyEM Project Team, Howard Hughes Medical Institute, Janelia Research Campus Ashburn, VA, USA.

ABSTRACT
Synaptic circuits for identified behaviors in the Drosophila brain have typically been considered from either a developmental or functional perspective without reference to how the circuits might have been inherited from ancestral forms. For example, two candidate pathways for ON- and OFF-edge motion detection in the visual system act via circuits that use respectively either T4 or T5, two cell types of the fourth neuropil, or lobula plate (LOP), that exhibit narrow-field direction-selective responses and provide input to wide-field tangential neurons. T4 or T5 both have four subtypes that terminate one each in the four strata of the LOP. Representatives are reported in a wide range of Diptera, and both cell types exhibit various similarities in: (1) the morphology of their dendritic arbors; (2) their four morphological and functional subtypes; (3) their cholinergic profile in Drosophila; (4) their input from the pathways of L3 cells in the first neuropil, or lamina (LA), and by one of a pair of LA cells, L1 (to the T4 pathway) and L2 (to the T5 pathway); and (5) their innervation by a single, wide-field contralateral tangential neuron from the central brain. Progenitors of both also express the gene atonal early in their proliferation from the inner anlage of the developing optic lobe, being alone among many other cell type progeny to do so. Yet T4 receives input in the second neuropil, or medulla (ME), and T5 in the third neuropil or lobula (LO). Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate ME and LO neuropils, and that a fiber crossing-the internal chiasma-arose between the two neuropils. The split most plausibly occurred, we suggest, with the formation of the LO as a new neuropil that formed when it separated from its ancestral neuropil to leave the ME, suggesting additionally that ME input neurons to T4 and T5 may also have had a common origin.

No MeSH data available.


The morphology of T4, T5, and complex tangential cell (CT1) cells. (A,B) Innervation patterns of T4 and T5 cells. VT37588-Gal4 driven Green Fluorescent Protein GFP(T2), mCD8::GFP (LL6) highlights the dendritic zone in ME stratum M10 for T4 dendrites and GR42H07-Gal4 driven GFP(T2), mCD8::GFP (LL6) highlights the dendritic zone in LO stratum Lo1 for T5 dendrites. Cell bodies (CB) intermingle in the cortex of the LOP; ME: medulla; LO: lobula. Background immunolabel: nc82 (anti-BRP, magenta). (C,D) Innervation patterns of single T4 and T5 cells (after Fischbach and Dittrich, 1989). The presynaptic (output) sites of the cells in the LOP are indicated in orange. Strata housing the dendritic (input) arbors are highlighted in pink [M10 in (C) and Lo1 in (D)]. In each cell type, four subtypes (a, b, c and d) each target one of the LOP’s four strata, Lop1, Lop2, Lop3 and Lop4. Only three T4 subtypes are shown in (C), as originally illustrated by Fischbach and Dittrich (1989). (E) Coronal projection of the CT1 cell. A bilateral pair of CB lies one each on either side of the midline (yellow dashed line), somewhat dorsal to the antennal lobes (white arrowheads). The axons project contralaterally, crossing each other at the midline (arrow) and medial to the optic lobe they bifurcate (black arrowhead) into a ME and a LO fiber. Columnar terminals are visible as a repeated array in strata M10 and Lo1. Blue and red: single cell flip-out clone for each CT1 cell (Nern et al., 2015); magenta: synaptotagmin-hemaglutinin (Syt-HA) indicating presynaptic sites; background immunolabel: nc82 (gray). (F) Innervation of CT1 in the optic lobe, seen in a horizontal plane. A single CT1 cell innervates the M10 and Lo1 strata, both in their entirety, communicating with T4 and T5 cells, respectively. Its axons run over the surface of the neuropils and project into them. A presynaptic marker Syt-HA expresses throughout both strata. Green: CT1-Gal4 driven GFP; yellow: Syt-HA; background immunolabel: nc82 (gray).
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Figure 2: The morphology of T4, T5, and complex tangential cell (CT1) cells. (A,B) Innervation patterns of T4 and T5 cells. VT37588-Gal4 driven Green Fluorescent Protein GFP(T2), mCD8::GFP (LL6) highlights the dendritic zone in ME stratum M10 for T4 dendrites and GR42H07-Gal4 driven GFP(T2), mCD8::GFP (LL6) highlights the dendritic zone in LO stratum Lo1 for T5 dendrites. Cell bodies (CB) intermingle in the cortex of the LOP; ME: medulla; LO: lobula. Background immunolabel: nc82 (anti-BRP, magenta). (C,D) Innervation patterns of single T4 and T5 cells (after Fischbach and Dittrich, 1989). The presynaptic (output) sites of the cells in the LOP are indicated in orange. Strata housing the dendritic (input) arbors are highlighted in pink [M10 in (C) and Lo1 in (D)]. In each cell type, four subtypes (a, b, c and d) each target one of the LOP’s four strata, Lop1, Lop2, Lop3 and Lop4. Only three T4 subtypes are shown in (C), as originally illustrated by Fischbach and Dittrich (1989). (E) Coronal projection of the CT1 cell. A bilateral pair of CB lies one each on either side of the midline (yellow dashed line), somewhat dorsal to the antennal lobes (white arrowheads). The axons project contralaterally, crossing each other at the midline (arrow) and medial to the optic lobe they bifurcate (black arrowhead) into a ME and a LO fiber. Columnar terminals are visible as a repeated array in strata M10 and Lo1. Blue and red: single cell flip-out clone for each CT1 cell (Nern et al., 2015); magenta: synaptotagmin-hemaglutinin (Syt-HA) indicating presynaptic sites; background immunolabel: nc82 (gray). (F) Innervation of CT1 in the optic lobe, seen in a horizontal plane. A single CT1 cell innervates the M10 and Lo1 strata, both in their entirety, communicating with T4 and T5 cells, respectively. Its axons run over the surface of the neuropils and project into them. A presynaptic marker Syt-HA expresses throughout both strata. Green: CT1-Gal4 driven GFP; yellow: Syt-HA; background immunolabel: nc82 (gray).

Mentions: The morphologies of T4 and T5 cells are highly characteristic, and each has unmistakable similarities to the other (Figures 2A–D) especially in the trajectory of its axon and the branching pattern of its dendrites. In fact, morphological similarities between the branching patterns of their dendritic arbors only make it more clear of the major difference between T4 and T5: the location of the arbor itself. This invades ME stratum M10 in the case of T4 or LO stratum Lo1 for T5 (Figures 2C,D).


A common evolutionary origin for the ON- and OFF-edge motion detection pathways of the Drosophila visual system.

Shinomiya K, Takemura SY, Rivlin PK, Plaza SM, Scheffer LK, Meinertzhagen IA - Front Neural Circuits (2015)

The morphology of T4, T5, and complex tangential cell (CT1) cells. (A,B) Innervation patterns of T4 and T5 cells. VT37588-Gal4 driven Green Fluorescent Protein GFP(T2), mCD8::GFP (LL6) highlights the dendritic zone in ME stratum M10 for T4 dendrites and GR42H07-Gal4 driven GFP(T2), mCD8::GFP (LL6) highlights the dendritic zone in LO stratum Lo1 for T5 dendrites. Cell bodies (CB) intermingle in the cortex of the LOP; ME: medulla; LO: lobula. Background immunolabel: nc82 (anti-BRP, magenta). (C,D) Innervation patterns of single T4 and T5 cells (after Fischbach and Dittrich, 1989). The presynaptic (output) sites of the cells in the LOP are indicated in orange. Strata housing the dendritic (input) arbors are highlighted in pink [M10 in (C) and Lo1 in (D)]. In each cell type, four subtypes (a, b, c and d) each target one of the LOP’s four strata, Lop1, Lop2, Lop3 and Lop4. Only three T4 subtypes are shown in (C), as originally illustrated by Fischbach and Dittrich (1989). (E) Coronal projection of the CT1 cell. A bilateral pair of CB lies one each on either side of the midline (yellow dashed line), somewhat dorsal to the antennal lobes (white arrowheads). The axons project contralaterally, crossing each other at the midline (arrow) and medial to the optic lobe they bifurcate (black arrowhead) into a ME and a LO fiber. Columnar terminals are visible as a repeated array in strata M10 and Lo1. Blue and red: single cell flip-out clone for each CT1 cell (Nern et al., 2015); magenta: synaptotagmin-hemaglutinin (Syt-HA) indicating presynaptic sites; background immunolabel: nc82 (gray). (F) Innervation of CT1 in the optic lobe, seen in a horizontal plane. A single CT1 cell innervates the M10 and Lo1 strata, both in their entirety, communicating with T4 and T5 cells, respectively. Its axons run over the surface of the neuropils and project into them. A presynaptic marker Syt-HA expresses throughout both strata. Green: CT1-Gal4 driven GFP; yellow: Syt-HA; background immunolabel: nc82 (gray).
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Related In: Results  -  Collection

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Figure 2: The morphology of T4, T5, and complex tangential cell (CT1) cells. (A,B) Innervation patterns of T4 and T5 cells. VT37588-Gal4 driven Green Fluorescent Protein GFP(T2), mCD8::GFP (LL6) highlights the dendritic zone in ME stratum M10 for T4 dendrites and GR42H07-Gal4 driven GFP(T2), mCD8::GFP (LL6) highlights the dendritic zone in LO stratum Lo1 for T5 dendrites. Cell bodies (CB) intermingle in the cortex of the LOP; ME: medulla; LO: lobula. Background immunolabel: nc82 (anti-BRP, magenta). (C,D) Innervation patterns of single T4 and T5 cells (after Fischbach and Dittrich, 1989). The presynaptic (output) sites of the cells in the LOP are indicated in orange. Strata housing the dendritic (input) arbors are highlighted in pink [M10 in (C) and Lo1 in (D)]. In each cell type, four subtypes (a, b, c and d) each target one of the LOP’s four strata, Lop1, Lop2, Lop3 and Lop4. Only three T4 subtypes are shown in (C), as originally illustrated by Fischbach and Dittrich (1989). (E) Coronal projection of the CT1 cell. A bilateral pair of CB lies one each on either side of the midline (yellow dashed line), somewhat dorsal to the antennal lobes (white arrowheads). The axons project contralaterally, crossing each other at the midline (arrow) and medial to the optic lobe they bifurcate (black arrowhead) into a ME and a LO fiber. Columnar terminals are visible as a repeated array in strata M10 and Lo1. Blue and red: single cell flip-out clone for each CT1 cell (Nern et al., 2015); magenta: synaptotagmin-hemaglutinin (Syt-HA) indicating presynaptic sites; background immunolabel: nc82 (gray). (F) Innervation of CT1 in the optic lobe, seen in a horizontal plane. A single CT1 cell innervates the M10 and Lo1 strata, both in their entirety, communicating with T4 and T5 cells, respectively. Its axons run over the surface of the neuropils and project into them. A presynaptic marker Syt-HA expresses throughout both strata. Green: CT1-Gal4 driven GFP; yellow: Syt-HA; background immunolabel: nc82 (gray).
Mentions: The morphologies of T4 and T5 cells are highly characteristic, and each has unmistakable similarities to the other (Figures 2A–D) especially in the trajectory of its axon and the branching pattern of its dendrites. In fact, morphological similarities between the branching patterns of their dendritic arbors only make it more clear of the major difference between T4 and T5: the location of the arbor itself. This invades ME stratum M10 in the case of T4 or LO stratum Lo1 for T5 (Figures 2C,D).

Bottom Line: Yet T4 receives input in the second neuropil, or medulla (ME), and T5 in the third neuropil or lobula (LO).Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate ME and LO neuropils, and that a fiber crossing-the internal chiasma-arose between the two neuropils.The split most plausibly occurred, we suggest, with the formation of the LO as a new neuropil that formed when it separated from its ancestral neuropil to leave the ME, suggesting additionally that ME input neurons to T4 and T5 may also have had a common origin.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology and Neuroscience, Life Sciences Centre, Dalhousie University Halifax, NS, Canada ; FlyEM Project Team, Howard Hughes Medical Institute, Janelia Research Campus Ashburn, VA, USA.

ABSTRACT
Synaptic circuits for identified behaviors in the Drosophila brain have typically been considered from either a developmental or functional perspective without reference to how the circuits might have been inherited from ancestral forms. For example, two candidate pathways for ON- and OFF-edge motion detection in the visual system act via circuits that use respectively either T4 or T5, two cell types of the fourth neuropil, or lobula plate (LOP), that exhibit narrow-field direction-selective responses and provide input to wide-field tangential neurons. T4 or T5 both have four subtypes that terminate one each in the four strata of the LOP. Representatives are reported in a wide range of Diptera, and both cell types exhibit various similarities in: (1) the morphology of their dendritic arbors; (2) their four morphological and functional subtypes; (3) their cholinergic profile in Drosophila; (4) their input from the pathways of L3 cells in the first neuropil, or lamina (LA), and by one of a pair of LA cells, L1 (to the T4 pathway) and L2 (to the T5 pathway); and (5) their innervation by a single, wide-field contralateral tangential neuron from the central brain. Progenitors of both also express the gene atonal early in their proliferation from the inner anlage of the developing optic lobe, being alone among many other cell type progeny to do so. Yet T4 receives input in the second neuropil, or medulla (ME), and T5 in the third neuropil or lobula (LO). Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate ME and LO neuropils, and that a fiber crossing-the internal chiasma-arose between the two neuropils. The split most plausibly occurred, we suggest, with the formation of the LO as a new neuropil that formed when it separated from its ancestral neuropil to leave the ME, suggesting additionally that ME input neurons to T4 and T5 may also have had a common origin.

No MeSH data available.