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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.


Two models for the origin of the lobula (LO) and internal chiasma. (A) (1) Hypothetical ancestral form. Medulla (ME) neuron antecedents to Mi and Tm neurons (red) in the ancestral ME/LO receive input in distal strata and provide input to undifferentiated ancestral T4/T5 LOP cells (blue). These cell pairs constitute two combined classes that are not initially differentiated, but which later duplicate. Gray arrows in each neuropil indicate direction of accretion of new columns to the neuropil, from first to last, corresponding to the posterior-anterior axis of the visual field; (2) T4/T5 cells duplicate, and their dendritic zone (pink) segregates into two. Then ingrowing Tm terminals separate the two layers between what will become the M10 and Lo1 strata, one for each differentiated T4 and T5 cell type, respectively. The original ME and the newly developed LO strata are thus arranged in tandem; (3) The newly formed LO separates from the ME, segregating T5 from T4 cell populations, and generating what will become the internal chiasma; (4) The LO rotates 90° in a counter-clockwise direction (gray dashed arrow in A3), the Tm axons (red) generating a chiasma between the ME and LO. Now the Tm cell axons must have changed the direction of their entry to the LO, to enable the LO to become rotated to its current position, parallel to the LOP. This causes the chiasma to form between ME and LO. (B) Alternative “VPN-duplication” model. Model A offers an explanation for the close similarity between ME stratum M10 (with T4 dendrites) and LO stratum Lo1 (with T5 dendrites), but not for the chiasma of Tm cell axons between them. (1) Ancestral form as in A1, but with additional projections from ancestral columnar VPNs in the proximal ME to the central brain. The numbers on the VPN CB represent the order of cell generation from a proposed proliferation center (1 = early, 4 = late). The direction of cell displacement is shown by a white arrow; (2) Some classes of VPNs may have duplicated in an anti-parallel direction (white arrows), originating from the proliferation center. It is proposed that the formation of a new neuropil, the LO (dashed black box), was induced by newly generated VPN populations. The polarity of the LO could then be defined by the order of VPN generation, as in the ME (Figure 1); (3) LO is now innervated by Tm cells from ME, which were generated by the duplication of Mi cells, as well as by T5 cells from LOP. Insofar as the anterior-posterior axis is inverted in LO from ME, the axons of Tm cells have to cross to innervate LO, causing the inner chiasma to form.
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Figure 4: Two models for the origin of the lobula (LO) and internal chiasma. (A) (1) Hypothetical ancestral form. Medulla (ME) neuron antecedents to Mi and Tm neurons (red) in the ancestral ME/LO receive input in distal strata and provide input to undifferentiated ancestral T4/T5 LOP cells (blue). These cell pairs constitute two combined classes that are not initially differentiated, but which later duplicate. Gray arrows in each neuropil indicate direction of accretion of new columns to the neuropil, from first to last, corresponding to the posterior-anterior axis of the visual field; (2) T4/T5 cells duplicate, and their dendritic zone (pink) segregates into two. Then ingrowing Tm terminals separate the two layers between what will become the M10 and Lo1 strata, one for each differentiated T4 and T5 cell type, respectively. The original ME and the newly developed LO strata are thus arranged in tandem; (3) The newly formed LO separates from the ME, segregating T5 from T4 cell populations, and generating what will become the internal chiasma; (4) The LO rotates 90° in a counter-clockwise direction (gray dashed arrow in A3), the Tm axons (red) generating a chiasma between the ME and LO. Now the Tm cell axons must have changed the direction of their entry to the LO, to enable the LO to become rotated to its current position, parallel to the LOP. This causes the chiasma to form between ME and LO. (B) Alternative “VPN-duplication” model. Model A offers an explanation for the close similarity between ME stratum M10 (with T4 dendrites) and LO stratum Lo1 (with T5 dendrites), but not for the chiasma of Tm cell axons between them. (1) Ancestral form as in A1, but with additional projections from ancestral columnar VPNs in the proximal ME to the central brain. The numbers on the VPN CB represent the order of cell generation from a proposed proliferation center (1 = early, 4 = late). The direction of cell displacement is shown by a white arrow; (2) Some classes of VPNs may have duplicated in an anti-parallel direction (white arrows), originating from the proliferation center. It is proposed that the formation of a new neuropil, the LO (dashed black box), was induced by newly generated VPN populations. The polarity of the LO could then be defined by the order of VPN generation, as in the ME (Figure 1); (3) LO is now innervated by Tm cells from ME, which were generated by the duplication of Mi cells, as well as by T5 cells from LOP. Insofar as the anterior-posterior axis is inverted in LO from ME, the axons of Tm cells have to cross to innervate LO, causing the inner chiasma to form.

Mentions: From the weight of evidence presented above, we next propose that T4 and T5 are in fact evolutionary siblings that derived from a common ancestral cell population, and that it is this path of descent from a single ancestral T4/T5 cell type that supports their deeper similarities, rather than, say, the functional roles that each cell type had to play to generate opponent ON- and OFF-edge motion pathways. A number of issues immediately present themselves: (1) how the LO arose, and whether, as we are about to suggest, this could have been from an ancestral neuropil fused with what then became the modern proximal medulla (PM); (2) the topological requirements for this transition, especially those of axon trajectories within the internal chiasma (Figure 4); and (3) the evolution or co-option of T4 and T5’s input neurons especially from different types of ME cells. We now consider these three questions in greater detail.


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)

Two models for the origin of the lobula (LO) and internal chiasma. (A) (1) Hypothetical ancestral form. Medulla (ME) neuron antecedents to Mi and Tm neurons (red) in the ancestral ME/LO receive input in distal strata and provide input to undifferentiated ancestral T4/T5 LOP cells (blue). These cell pairs constitute two combined classes that are not initially differentiated, but which later duplicate. Gray arrows in each neuropil indicate direction of accretion of new columns to the neuropil, from first to last, corresponding to the posterior-anterior axis of the visual field; (2) T4/T5 cells duplicate, and their dendritic zone (pink) segregates into two. Then ingrowing Tm terminals separate the two layers between what will become the M10 and Lo1 strata, one for each differentiated T4 and T5 cell type, respectively. The original ME and the newly developed LO strata are thus arranged in tandem; (3) The newly formed LO separates from the ME, segregating T5 from T4 cell populations, and generating what will become the internal chiasma; (4) The LO rotates 90° in a counter-clockwise direction (gray dashed arrow in A3), the Tm axons (red) generating a chiasma between the ME and LO. Now the Tm cell axons must have changed the direction of their entry to the LO, to enable the LO to become rotated to its current position, parallel to the LOP. This causes the chiasma to form between ME and LO. (B) Alternative “VPN-duplication” model. Model A offers an explanation for the close similarity between ME stratum M10 (with T4 dendrites) and LO stratum Lo1 (with T5 dendrites), but not for the chiasma of Tm cell axons between them. (1) Ancestral form as in A1, but with additional projections from ancestral columnar VPNs in the proximal ME to the central brain. The numbers on the VPN CB represent the order of cell generation from a proposed proliferation center (1 = early, 4 = late). The direction of cell displacement is shown by a white arrow; (2) Some classes of VPNs may have duplicated in an anti-parallel direction (white arrows), originating from the proliferation center. It is proposed that the formation of a new neuropil, the LO (dashed black box), was induced by newly generated VPN populations. The polarity of the LO could then be defined by the order of VPN generation, as in the ME (Figure 1); (3) LO is now innervated by Tm cells from ME, which were generated by the duplication of Mi cells, as well as by T5 cells from LOP. Insofar as the anterior-posterior axis is inverted in LO from ME, the axons of Tm cells have to cross to innervate LO, causing the inner chiasma to form.
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Related In: Results  -  Collection

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Figure 4: Two models for the origin of the lobula (LO) and internal chiasma. (A) (1) Hypothetical ancestral form. Medulla (ME) neuron antecedents to Mi and Tm neurons (red) in the ancestral ME/LO receive input in distal strata and provide input to undifferentiated ancestral T4/T5 LOP cells (blue). These cell pairs constitute two combined classes that are not initially differentiated, but which later duplicate. Gray arrows in each neuropil indicate direction of accretion of new columns to the neuropil, from first to last, corresponding to the posterior-anterior axis of the visual field; (2) T4/T5 cells duplicate, and their dendritic zone (pink) segregates into two. Then ingrowing Tm terminals separate the two layers between what will become the M10 and Lo1 strata, one for each differentiated T4 and T5 cell type, respectively. The original ME and the newly developed LO strata are thus arranged in tandem; (3) The newly formed LO separates from the ME, segregating T5 from T4 cell populations, and generating what will become the internal chiasma; (4) The LO rotates 90° in a counter-clockwise direction (gray dashed arrow in A3), the Tm axons (red) generating a chiasma between the ME and LO. Now the Tm cell axons must have changed the direction of their entry to the LO, to enable the LO to become rotated to its current position, parallel to the LOP. This causes the chiasma to form between ME and LO. (B) Alternative “VPN-duplication” model. Model A offers an explanation for the close similarity between ME stratum M10 (with T4 dendrites) and LO stratum Lo1 (with T5 dendrites), but not for the chiasma of Tm cell axons between them. (1) Ancestral form as in A1, but with additional projections from ancestral columnar VPNs in the proximal ME to the central brain. The numbers on the VPN CB represent the order of cell generation from a proposed proliferation center (1 = early, 4 = late). The direction of cell displacement is shown by a white arrow; (2) Some classes of VPNs may have duplicated in an anti-parallel direction (white arrows), originating from the proliferation center. It is proposed that the formation of a new neuropil, the LO (dashed black box), was induced by newly generated VPN populations. The polarity of the LO could then be defined by the order of VPN generation, as in the ME (Figure 1); (3) LO is now innervated by Tm cells from ME, which were generated by the duplication of Mi cells, as well as by T5 cells from LOP. Insofar as the anterior-posterior axis is inverted in LO from ME, the axons of Tm cells have to cross to innervate LO, causing the inner chiasma to form.
Mentions: From the weight of evidence presented above, we next propose that T4 and T5 are in fact evolutionary siblings that derived from a common ancestral cell population, and that it is this path of descent from a single ancestral T4/T5 cell type that supports their deeper similarities, rather than, say, the functional roles that each cell type had to play to generate opponent ON- and OFF-edge motion pathways. A number of issues immediately present themselves: (1) how the LO arose, and whether, as we are about to suggest, this could have been from an ancestral neuropil fused with what then became the modern proximal medulla (PM); (2) the topological requirements for this transition, especially those of axon trajectories within the internal chiasma (Figure 4); and (3) the evolution or co-option of T4 and T5’s input neurons especially from different types of ME cells. We now consider these three questions in greater detail.

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.