Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex

Abstract

The representation and integration of internal and external cues is crucial for any organism to execute appropriate behaviors. In insects, a highly conserved region of the brain, the central complex (CX), functions in the representation of spatial information and behavioral states, as well as the transformation of this information into desired navigational commands. How does this relatively invariant structure enable the incorporation of information from the diversity of anatomical, behavioral, and ecological niches occupied by insects? Here, we examine the input channels to the CX in the context of their development and evolution. Insect brains develop from ~ 100 neuroblasts per hemisphere that divide systematically to form “lineages” of sister neurons, that project to their target neuropils along anatomically characteristic tracts. Overlaying this developmental tract information onto the recently generated Drosophila “hemibrain” connectome and integrating this information with the anatomical and physiological recording of neurons in other species, we observe neuropil and lineage-specific innervation, connectivity, and activity profiles in CX input channels. We posit that the proliferative potential of neuroblasts and the lineage-based architecture of information channels enable the modification of neural networks across existing, novel, and deprecated modalities in a species-specific manner, thus forming the substrate for the evolution and diversification of insect navigational circuits.

Stem cell-specific ecdysone signaling regulates the development and function of aDrosophilasleep homeostat

“…Previous clonal studies could not find any contributions of DM1 lineage to the long-field input neurons. However, consistent with our findings, a recent connectomics-based lineage assignment study has also proposed DM1 lineage contribution to the FB tangential input neurons 101 . Although all ~12 neurons look similar in morphology, our clonal analysis data suggests a likely heterogeneity of cells in this cluster.…”

“…Previous studies have assigned a unique clone morphology to each NSC present in the larval central brain, thus providing a reference framework for the clonal developmental organization of the adult Drosophila brain 63,64,68 . The DM1-4 Type II NSCs generate most local columnar neurons, and DL1 generates the majority of long-filed tangential input neurons with a minor contribution from DM4 and 6 63,64,101 . To determine which Type II NSCs generate dFB neurons, we used a heat shock-based lineage filtering method called cell class-lineage analysis (CLIn) 102 .…”

“…The FB is the most diverse structure of the CX neuropils, which receives input from the periphery via the long-field neurons that innervate different FB layers topographically. The FB long-field neurons arise from diverse NSCs, with significant contributions from the DL1 Type II NSC and DALc12v Type I NSC 63,64,68,101 . The sleep-promoting dFB neurons are long-field input neurons that innervate layers six-seven of the FB 36 .…”

Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster

“…Our lineage-associated tracts have been mapped by light microscopy and assigned to named lineage clones. 139 , 199 , 200 , 201 , 202 We have discovered them in the adult brain FAFB dataset. 50 Lacin et al.…”

“…We thank Clare Pilgrim, Alex McLachlan and David Osumi-Sutherland for incorporating our predictions into Virtual Fly Brain. Researchers 18 , 50 , 65 , 74 , 76 , 90 , 114 , 202 , 208 , 209 , 210 , 211 have already utilized our preprinted results to formulate neurobiological hypotheses. The most reliable predictions align across hemispheres, exhibit cohesion within a cell type, adhere to Lacin’s law and remain consistent across datasets.…”