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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.


Possible origins of ME cell inputs to T4 and T5. (A,B) Profiles of Mi1 and Tm3 (L1 pathway, green) and Tm1, 2 and 4 (L2 pathway, orange), from Golgi impregnations (after Fischbach and Dittrich, 1989). Tm3 and Tm4 are proposed to have arisen by duplication, and extend axons to terminals in the LO. (C) The original T4/T5 cell population of an ancestral fused ME/LO is proposed to have received input from an ancestral ME intrinsic (Mi) neuron from which later Tm cells derived. Gray arrows indicate direction of accretion of new columns to the neuropil, corresponding to the posterior-anterior axis of the visual field (cf. Figure 4A). (D) When the LO separated from the inner layers of the ME, Tm1 and Tm2 cells are proposed to have derived from the Mi cells, losing their connection with the T cells in stratum M10 but retaining synaptic connection with newly differentiated T5 cells in LO stratum Lo1. The Mi cell type survived as Mi1. (E) The LO split from the ancestral ME. The axon of the Tm1/Tm2 cells entered the LO from its distal end and terminated in Lo1, located on one side of the ME. (F) Tm cell axons enter the LO from the side of the LOP. In a final step, Tm1/Tm2 segregate into two separate Tm cell types, both retaining input from L2.
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Figure 5: Possible origins of ME cell inputs to T4 and T5. (A,B) Profiles of Mi1 and Tm3 (L1 pathway, green) and Tm1, 2 and 4 (L2 pathway, orange), from Golgi impregnations (after Fischbach and Dittrich, 1989). Tm3 and Tm4 are proposed to have arisen by duplication, and extend axons to terminals in the LO. (C) The original T4/T5 cell population of an ancestral fused ME/LO is proposed to have received input from an ancestral ME intrinsic (Mi) neuron from which later Tm cells derived. Gray arrows indicate direction of accretion of new columns to the neuropil, corresponding to the posterior-anterior axis of the visual field (cf. Figure 4A). (D) When the LO separated from the inner layers of the ME, Tm1 and Tm2 cells are proposed to have derived from the Mi cells, losing their connection with the T cells in stratum M10 but retaining synaptic connection with newly differentiated T5 cells in LO stratum Lo1. The Mi cell type survived as Mi1. (E) The LO split from the ancestral ME. The axon of the Tm1/Tm2 cells entered the LO from its distal end and terminated in Lo1, located on one side of the ME. (F) Tm cell axons enter the LO from the side of the LOP. In a final step, Tm1/Tm2 segregate into two separate Tm cell types, both retaining input from L2.

Mentions: The easiest case to imagine is that in the model shown in Figure 4A, because the dendrites of both new cell types would initially have been closely associated, and at least some input neurons to T4 and T5 should be equivalent sibling descendants. The Tm3 inputs to T4 and the Tm4 inputs to T5 provide the most obvious case, with Tm3 providing input in stratum M10 and Tm4 in stratum Lo1 (Figure 5A). Both also provide inputs to the deeper LO stratum Lo4, but to unknown targets there (for Tm4: Shinomiya et al., 2014). We suggest that these two cell types arose by duplication from a single input innervating the ancestral T4/T5 population in the antecedent ME, each cell type then developing its own individual dendrites and arbors in the ME and deeper in the LO, and eventually terminating in stratum Lo4 (Figure 5A). Mi9 and Tm9 input is another obvious case (Figure 3). Suggesting their common ancestry, both ME cells receive input from the same LA cell type, L3 (Takemura et al., 2013).


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)

Possible origins of ME cell inputs to T4 and T5. (A,B) Profiles of Mi1 and Tm3 (L1 pathway, green) and Tm1, 2 and 4 (L2 pathway, orange), from Golgi impregnations (after Fischbach and Dittrich, 1989). Tm3 and Tm4 are proposed to have arisen by duplication, and extend axons to terminals in the LO. (C) The original T4/T5 cell population of an ancestral fused ME/LO is proposed to have received input from an ancestral ME intrinsic (Mi) neuron from which later Tm cells derived. Gray arrows indicate direction of accretion of new columns to the neuropil, corresponding to the posterior-anterior axis of the visual field (cf. Figure 4A). (D) When the LO separated from the inner layers of the ME, Tm1 and Tm2 cells are proposed to have derived from the Mi cells, losing their connection with the T cells in stratum M10 but retaining synaptic connection with newly differentiated T5 cells in LO stratum Lo1. The Mi cell type survived as Mi1. (E) The LO split from the ancestral ME. The axon of the Tm1/Tm2 cells entered the LO from its distal end and terminated in Lo1, located on one side of the ME. (F) Tm cell axons enter the LO from the side of the LOP. In a final step, Tm1/Tm2 segregate into two separate Tm cell types, both retaining input from L2.
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Figure 5: Possible origins of ME cell inputs to T4 and T5. (A,B) Profiles of Mi1 and Tm3 (L1 pathway, green) and Tm1, 2 and 4 (L2 pathway, orange), from Golgi impregnations (after Fischbach and Dittrich, 1989). Tm3 and Tm4 are proposed to have arisen by duplication, and extend axons to terminals in the LO. (C) The original T4/T5 cell population of an ancestral fused ME/LO is proposed to have received input from an ancestral ME intrinsic (Mi) neuron from which later Tm cells derived. Gray arrows indicate direction of accretion of new columns to the neuropil, corresponding to the posterior-anterior axis of the visual field (cf. Figure 4A). (D) When the LO separated from the inner layers of the ME, Tm1 and Tm2 cells are proposed to have derived from the Mi cells, losing their connection with the T cells in stratum M10 but retaining synaptic connection with newly differentiated T5 cells in LO stratum Lo1. The Mi cell type survived as Mi1. (E) The LO split from the ancestral ME. The axon of the Tm1/Tm2 cells entered the LO from its distal end and terminated in Lo1, located on one side of the ME. (F) Tm cell axons enter the LO from the side of the LOP. In a final step, Tm1/Tm2 segregate into two separate Tm cell types, both retaining input from L2.
Mentions: The easiest case to imagine is that in the model shown in Figure 4A, because the dendrites of both new cell types would initially have been closely associated, and at least some input neurons to T4 and T5 should be equivalent sibling descendants. The Tm3 inputs to T4 and the Tm4 inputs to T5 provide the most obvious case, with Tm3 providing input in stratum M10 and Tm4 in stratum Lo1 (Figure 5A). Both also provide inputs to the deeper LO stratum Lo4, but to unknown targets there (for Tm4: Shinomiya et al., 2014). We suggest that these two cell types arose by duplication from a single input innervating the ancestral T4/T5 population in the antecedent ME, each cell type then developing its own individual dendrites and arbors in the ME and deeper in the LO, and eventually terminating in stratum Lo4 (Figure 5A). Mi9 and Tm9 input is another obvious case (Figure 3). Suggesting their common ancestry, both ME cells receive input from the same LA cell type, L3 (Takemura et al., 2013).

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.