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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 formation of lamina (LA) and medulla (ME) neuropils by duplication from a single proliferation center, or neuroblast (Nb) anlage. Cells of the LA and ME cortices proliferate in antiparallel directions from this center, their axons growing in temporal sequence between the two (see: e.g., Figure 3 in Meinertzhagen, 1973). A crossed fiber tract, the external chiasma, necessarily forms between the two as the coordinated outcome of two events, cell proliferation into LA and ME cortices in antiparallel directions, and the directed growth of axons so as to penetrate the LA but grow across the face of the ME. The retinotopic sequence of innervation of the LA matches the order of projection of ME cells to the lobula (LO).
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Figure 1: The formation of lamina (LA) and medulla (ME) neuropils by duplication from a single proliferation center, or neuroblast (Nb) anlage. Cells of the LA and ME cortices proliferate in antiparallel directions from this center, their axons growing in temporal sequence between the two (see: e.g., Figure 3 in Meinertzhagen, 1973). A crossed fiber tract, the external chiasma, necessarily forms between the two as the coordinated outcome of two events, cell proliferation into LA and ME cortices in antiparallel directions, and the directed growth of axons so as to penetrate the LA but grow across the face of the ME. The retinotopic sequence of innervation of the LA matches the order of projection of ME cells to the lobula (LO).

Mentions: In the case of the two outermost optic neuropils in arthropods, the first optic neuropil—or lamina (LA)—and the outer part of the second neuropil, or medulla (ME), neuropil splitting is said to have occurred among neuroblast proliferation centers, or anlagen, and to be accompanied by the formation of a chiasma of axons connecting between the two new descendant neuropils (Strausfeld, 2005, 2009). The formation of the external chiasma required that LA cell axons grow down the face of the ME rather than penetrating it in a direction normal to its surface (Elofsson and Dahl, 1970; Meinertzhagen, 1973), as do photoreceptor axons that innervate the LA from the eye (Figure 1). A chiasma is in that case the inevitable topological outcome, one that preserves retinotopy but inverts it.


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 formation of lamina (LA) and medulla (ME) neuropils by duplication from a single proliferation center, or neuroblast (Nb) anlage. Cells of the LA and ME cortices proliferate in antiparallel directions from this center, their axons growing in temporal sequence between the two (see: e.g., Figure 3 in Meinertzhagen, 1973). A crossed fiber tract, the external chiasma, necessarily forms between the two as the coordinated outcome of two events, cell proliferation into LA and ME cortices in antiparallel directions, and the directed growth of axons so as to penetrate the LA but grow across the face of the ME. The retinotopic sequence of innervation of the LA matches the order of projection of ME cells to the lobula (LO).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4496578&req=5

Figure 1: The formation of lamina (LA) and medulla (ME) neuropils by duplication from a single proliferation center, or neuroblast (Nb) anlage. Cells of the LA and ME cortices proliferate in antiparallel directions from this center, their axons growing in temporal sequence between the two (see: e.g., Figure 3 in Meinertzhagen, 1973). A crossed fiber tract, the external chiasma, necessarily forms between the two as the coordinated outcome of two events, cell proliferation into LA and ME cortices in antiparallel directions, and the directed growth of axons so as to penetrate the LA but grow across the face of the ME. The retinotopic sequence of innervation of the LA matches the order of projection of ME cells to the lobula (LO).
Mentions: In the case of the two outermost optic neuropils in arthropods, the first optic neuropil—or lamina (LA)—and the outer part of the second neuropil, or medulla (ME), neuropil splitting is said to have occurred among neuroblast proliferation centers, or anlagen, and to be accompanied by the formation of a chiasma of axons connecting between the two new descendant neuropils (Strausfeld, 2005, 2009). The formation of the external chiasma required that LA cell axons grow down the face of the ME rather than penetrating it in a direction normal to its surface (Elofsson and Dahl, 1970; Meinertzhagen, 1973), as do photoreceptor axons that innervate the LA from the eye (Figure 1). A chiasma is in that case the inevitable topological outcome, one that preserves retinotopy but inverts it.

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.