Flexible behaviors over long timescales are thought to engage recurrent neural networks in deep brain regions, which are experimentally challenging to study. In insects, recurrent circuit dynamics in a brain region called the central complex (CX) enable directed locomotion, sleep, and context- and experience-dependent spatial navigation. We describe the first complete electron-microscopy-based connectome of the Drosophila CX, including all its neurons and circuits at synaptic resolution. We identified new CX neuron types, novel sensory and motor pathways, and network motifs that likely enable the CX to extract the fly9s head-direction, maintain it with attractor dynamics, and combine it with other sensorimotor information to perform vector-based navigational computations. We also identified numerous pathways that may facilitate the selection of CX-driven behavioral patterns by context and internal state. The CX connectome provides a comprehensive blueprint necessary for a detailed understanding of network dynamics underlying sleep, flexible navigation, and state-dependent action selection.

https://www.biorxiv.org/content/biorxiv/early/2020/12/09/2020.12.08.413955.full.pdf

A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection

The neuroanatomical ultrastructure and function of a biological ring attractor

Neural representations of head direction have been discovered in many different species. A large body of theoretical work has proposed that the dynamics associated with these representations might be generated, maintained, and updated by recurrent network structures called ring attractors. Ring attractor models rely on specific assumptions about the structure of excitatory and inhibitory connectivity. These assumptions have been difficult to test directly. We therefore performed electron-microscopy-based circuit reconstruction and RNA profiling of identified cell types in the heading direction system of Drosophila melanogaster to directly examine excitatory and inhibitory synaptic connectivity, generating a dataset that should serve as a reference for future functional studies of the network. Consistent with several theoretical models, we identified network motifs that have been hypothesized to maintain the heading representation in darkness, update it when the animal turns, and tether it to visual cues. Genetically targeted two-photon calcium imaging and thermogenetic perturbation of the constituent neuron types during behavior provided additional support for these functional roles. However, we also discovered network motifs absent in current models, including a surprising degree of recurrence between arbors of different neurons with mixed pre- and post-synaptic specializations. Overall, our results confirm that the Drosophila heading direction network contains the core components of a ring attractor while also revealing unpredicted structural features that might enable the heading system to accurately track the animal9s heading with a small number of neurons.

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Toward an insect evolution resolution Insects are the most diverse group of animals, with the largest number of species. However, many of the evolutionary relationships between insect species have been controversial and difficult to resolve. Misof et al. performed a phylogenomic analysis of protein-coding genes from all major insect orders and close relatives, resolving the placement of taxa. The authors used this resolved phylogenetic tree together with fossil analysis to date the origin of insects to ~479 million years ago and to resolve long-controversial subjects in insect phylogeny. Science, this issue p. 763 The phylogeny of all major insect lineages reveals how and when insects diversified. Insects are the most speciose group of animals, but the phylogenetic relationships of many major lineages remain unresolved. We inferred the phylogeny of insects from 1478 protein-coding genes. Phylogenomic analyses of nucleotide and amino acid sequences, with site-specific nucleotide or domain-specific amino acid substitution models, produced statistically robust and congruent results resolving previously controversial phylogenetic relations hips. We dated the origin of insects to the Early Ordovician [~479 million years ago (Ma)], of insect flight to the Early Devonian (~406 Ma), of major extant lineages to the Mississippian (~345 Ma), and the major diversification of holometabolous insects to the Early Cretaceous. Our phylogenomic study provides a comprehensive reliable scaffold for future comparative analyses of evolutionary innovations among insects.

Phylogenomics Resolves The Timing And Pattern Of Insect Evolution: Supplementary File Archives.

Many insects use patterns of polarized light in the sky to orient and navigate. Here, we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly's sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the 'sky compass' pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

A visual pathway for skylight polarization processing in Drosophila.

The central complex (CX) comprises a group of midline neuropils in the insect brain, consisting of the protocerebral bridge (PB), the upper (CBU) and lower division (CBL) of the central body and a pair of globular noduli. It receives prominent input from the visual system and plays a major role in spatial orientation of the animals. Vertical slices and horizontal layers of the CX are formed by columnar, tangential, and pontine neurons. While pontine and columnar neurons have been analyzed in detail, especially in the fruit fly and desert locust, understanding of the organization of tangential cells is still rudimentary. As a basis for future functional studies, we have studied the morphologies of tangential neurons of the CX of the desert locust Schistocerca gregaria. Intracellular dye injections revealed 43 different types of tangential neuron, 8 of the PB, 5 of the CBL, 24 of the CBU, 2 of the noduli, and 4 innervating multiple substructures. Cell bodies of these neurons were located in 11 different clusters in the cell body rind. Judging from the presence of fine versus beaded terminals, the vast majority of these neurons provide input into the CX, especially from the lateral complex (LX), the superior protocerebrum, the posterior slope, and other surrounding brain areas, but not directly from the mushroom bodies. Connections are largely subunit- and partly layer-specific. No direct connections were found between the CBU and the CBL. Instead, both subdivisions are connected in parallel with the PB and distinct layers of the noduli.

Neuroarchitecture of the central complex of the desert locust: Tangential neurons.

The central complex is a group of midline-crossing neuropils in the insect brain involved in head direction coding, sky compass navigation, and spatial visual memory. To compare the neuroarchitecture and neurochemistry of the central complex in insects that differ in locomotion, ways of orientation, time of activity (diurnal, nocturnal), and evolutionary history, we studied the distribution of γ-aminobutyric acid (GABA) immunostaining in the central complex of 29 species, ranging from Zygentoma to Diptera. In all species, the lower division of the central body was densely innervated by GABA-immunoreactive tangential neurons. These neurons had additional arborizations in the bulb, a distinct region of synaptic complexes in the lateral complex, and somata in a cell cluster mediodorsally to the antennal lobe. Differences in the appearance of GABA immunostaining in the lower division of the central body corresponded to differences in neuropil architecture, such as transformation of the lower division into a toroid in certain Diptera and Heteroptera. In nearly all species two additional systems of tangential neuron of the upper division of the central body were GABA-immunoreactive. One of these systems diffusely invaded a superior layer, while the second system showed fan-like projections in an inferior layer. Sparse immunostaining in the protocerebral bridge was detected in cockroaches, a cricket, and two hemipteran species. The data show that three systems of GABA-immunoreactive tangential neurons of the central body are highly conserved and suggest that the layered organization of the upper division of the central body is, likewise, largely maintained from basal to advanced species.

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Manuel Quintero Pérez

Papers

Neuroarchitecture of the central complex of the desert locust: Tangential neurons.

GABA immunostaining in the central complex of dicondylian insects.