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.
Highlights
The Evolution of Synaptic Circuits The problem of how a complex brain with highly organized pathways and centers could have arisen from simpler forms lacking clear structural compartments and with less differentiated cellular components, has generally attracted discussion in seeking a transition from very basal forms to those in which brain structure assumes some canonical stage (Arendt et al, 2008)
Some Consequences: if T4 and T5 were Evolutionary Sibling Cell Types From the weight of evidence presented above, we propose that T4 and T5 are 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 OFFedge motion pathways
In our interpretation the LO may have arisen, and so can be considered, as a duplicated structure of the Pm, to which it may initially have been fused in ancestral forms. We find these ‘‘duplication models’’ the easiest way to account for how two such similar cell types as T4 and T5 could be located in modern forms in these two neighboring neuropils
Summary
The Evolution of Synaptic Circuits The problem of how a complex brain with highly organized pathways and centers could have arisen from simpler forms lacking clear structural compartments and with less differentiated cellular components, has generally attracted discussion in seeking a transition from very basal forms to those in which brain structure assumes some canonical stage (Arendt et al, 2008). 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 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
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