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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.


Related in: MedlinePlus

The separate origins of the L1 and L2 pathways. (A) L1 and L2 are proposed to have originated by a duplication event involving their innervation by photoreceptor axons derived from the retina (RE). In the ancestral form, only a single subtype of LA (L) cell is proposed to have received input from the photoreceptor cells (R1–R6) in the LA and provide output to the ME, later through the external chiasma. Ancestral unicolumnar Mi cells are shown as a target of the L-cell terminal in the ME, and these provide input to a single type of ancestral T-cell that transferred motion information from the ME to the LOP, in parallel with the segregation of separate T4 and T5 cells. (B) L1 retained an ancestral unicolumnar target neuron that became Mi1, together with multicolumnar neurons that transformed into Tm3 neurons after the ancestral combined neuropil split to yield separate ME and LO neuropils. The ancestral T-cell differentiated into T4 cells, which mediate signals in the L1 pathway. L2’s target neurons transformed into Tm cells, one undergoing a further duplication to yield paired unicolumnar neurons Tm1 and Tm2, and Tm4, which transformed from an ancestral multicolumnar Mi neuron. The Tm cells extended axons to the newly generated LO, providing input to the T5 cell.
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Figure 6: The separate origins of the L1 and L2 pathways. (A) L1 and L2 are proposed to have originated by a duplication event involving their innervation by photoreceptor axons derived from the retina (RE). In the ancestral form, only a single subtype of LA (L) cell is proposed to have received input from the photoreceptor cells (R1–R6) in the LA and provide output to the ME, later through the external chiasma. Ancestral unicolumnar Mi cells are shown as a target of the L-cell terminal in the ME, and these provide input to a single type of ancestral T-cell that transferred motion information from the ME to the LOP, in parallel with the segregation of separate T4 and T5 cells. (B) L1 retained an ancestral unicolumnar target neuron that became Mi1, together with multicolumnar neurons that transformed into Tm3 neurons after the ancestral combined neuropil split to yield separate ME and LO neuropils. The ancestral T-cell differentiated into T4 cells, which mediate signals in the L1 pathway. L2’s target neurons transformed into Tm cells, one undergoing a further duplication to yield paired unicolumnar neurons Tm1 and Tm2, and Tm4, which transformed from an ancestral multicolumnar Mi neuron. The Tm cells extended axons to the newly generated LO, providing input to the T5 cell.

Mentions: Did L1 and L2 arise by duplication in the LA to initiate the segregation between T4 and T5? The circuits driving modern T4 and T5 differ in receiving respective inputs from the L1 and L2 pathways. How might these have arisen as separate pathways? Evidence is mostly only suggestive, but both L-cells are similar in two important ways. First, their dendrites cooperate closely in occupying two of the four postsynaptic sites at all photoreceptor tetrads (Meinertzhagen and O’Neil, 1991; Rivera-Alba et al., 2011), and second their axons are similar in occupying paired locations at the cartridge axis, in positions determined by the matched levels of their N-Cadherin (nCad) expression (Schwabe et al., 2014). Meinertzhagen and Shaw (1989) have previously proposed that the paired nature of L1 and L2 may reflect an original duplication event in these pathways (Figure 6), possibly so as to match the transcriptomes of these cells more closely to each other than to other LA cells, but certainly any duplication must have been long ago, presumably predating the segregation of T4 and T5 populations. Could a duplication in the L1 and L2 pathways have driven the downstream segregation between the T4 and T5 cells? Neurons homologous to L1 and L2 date back long periods of time even by geological standards. For example tetrad synapses and L1 and L2 counterparts also exist in the optic lobe of locusts (Wernitznig et al., 2015). So these features are now suggested to have developed in a common ancestor and be widely shared across neopteran species, probably dating back at least ~390 million years in the Devonian (Misof et al., 2014). Their proposed duplication has also been accompanied by a change in neurotransmitter phenotype, glutamate for L1 and acetylcholine for L2 (Takemura et al., 2011).


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 separate origins of the L1 and L2 pathways. (A) L1 and L2 are proposed to have originated by a duplication event involving their innervation by photoreceptor axons derived from the retina (RE). In the ancestral form, only a single subtype of LA (L) cell is proposed to have received input from the photoreceptor cells (R1–R6) in the LA and provide output to the ME, later through the external chiasma. Ancestral unicolumnar Mi cells are shown as a target of the L-cell terminal in the ME, and these provide input to a single type of ancestral T-cell that transferred motion information from the ME to the LOP, in parallel with the segregation of separate T4 and T5 cells. (B) L1 retained an ancestral unicolumnar target neuron that became Mi1, together with multicolumnar neurons that transformed into Tm3 neurons after the ancestral combined neuropil split to yield separate ME and LO neuropils. The ancestral T-cell differentiated into T4 cells, which mediate signals in the L1 pathway. L2’s target neurons transformed into Tm cells, one undergoing a further duplication to yield paired unicolumnar neurons Tm1 and Tm2, and Tm4, which transformed from an ancestral multicolumnar Mi neuron. The Tm cells extended axons to the newly generated LO, providing input to the T5 cell.
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Related In: Results  -  Collection

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Figure 6: The separate origins of the L1 and L2 pathways. (A) L1 and L2 are proposed to have originated by a duplication event involving their innervation by photoreceptor axons derived from the retina (RE). In the ancestral form, only a single subtype of LA (L) cell is proposed to have received input from the photoreceptor cells (R1–R6) in the LA and provide output to the ME, later through the external chiasma. Ancestral unicolumnar Mi cells are shown as a target of the L-cell terminal in the ME, and these provide input to a single type of ancestral T-cell that transferred motion information from the ME to the LOP, in parallel with the segregation of separate T4 and T5 cells. (B) L1 retained an ancestral unicolumnar target neuron that became Mi1, together with multicolumnar neurons that transformed into Tm3 neurons after the ancestral combined neuropil split to yield separate ME and LO neuropils. The ancestral T-cell differentiated into T4 cells, which mediate signals in the L1 pathway. L2’s target neurons transformed into Tm cells, one undergoing a further duplication to yield paired unicolumnar neurons Tm1 and Tm2, and Tm4, which transformed from an ancestral multicolumnar Mi neuron. The Tm cells extended axons to the newly generated LO, providing input to the T5 cell.
Mentions: Did L1 and L2 arise by duplication in the LA to initiate the segregation between T4 and T5? The circuits driving modern T4 and T5 differ in receiving respective inputs from the L1 and L2 pathways. How might these have arisen as separate pathways? Evidence is mostly only suggestive, but both L-cells are similar in two important ways. First, their dendrites cooperate closely in occupying two of the four postsynaptic sites at all photoreceptor tetrads (Meinertzhagen and O’Neil, 1991; Rivera-Alba et al., 2011), and second their axons are similar in occupying paired locations at the cartridge axis, in positions determined by the matched levels of their N-Cadherin (nCad) expression (Schwabe et al., 2014). Meinertzhagen and Shaw (1989) have previously proposed that the paired nature of L1 and L2 may reflect an original duplication event in these pathways (Figure 6), possibly so as to match the transcriptomes of these cells more closely to each other than to other LA cells, but certainly any duplication must have been long ago, presumably predating the segregation of T4 and T5 populations. Could a duplication in the L1 and L2 pathways have driven the downstream segregation between the T4 and T5 cells? Neurons homologous to L1 and L2 date back long periods of time even by geological standards. For example tetrad synapses and L1 and L2 counterparts also exist in the optic lobe of locusts (Wernitznig et al., 2015). So these features are now suggested to have developed in a common ancestor and be widely shared across neopteran species, probably dating back at least ~390 million years in the Devonian (Misof et al., 2014). Their proposed duplication has also been accompanied by a change in neurotransmitter phenotype, glutamate for L1 and acetylcholine for L2 (Takemura et al., 2011).

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.


Related in: MedlinePlus