The head direction circuit of two insect species

Abstract

Recent studies of the Central Complex in the brain of the fruit fly Drosophila melanogaster have identified neurons with localised activity that tracks the animal's heading direction. These neurons are part of a neuronal circuit with dynamics resembling those of a ring attractor. Other insects have a homologous circuit sharing a generally similar topographic structure but with significant structural and connectivity differences. In this study, we model the precise connectivity patterns in two insect species to investigate the effect of the differences on the dynamics of the circuit. We illustrate that the circuit found in locusts can also operate as a ring attractor and we explore the role and robustness of the connectivity parameters. We identify differences that enable the fruit fly circuit to respond faster to changes of heading while they render the locust circuit more tolerant to noise. Our findings demonstrate that subtle differences in neuronal projection patterns can have a significant effect on the circuit performance and emphasise the need for a comparative approach in neuroscience. 7 distractions [6], but is also essential for the more complex navigational process of path integration 8 (or dead reckoning) which enables central-place foragers to return directly to their nest after long 9 and convoluted outward paths [7][8][9][10]. While the neural basis underlying these navigation strategies 10 are not known in detail, a brain region called the central complex (CX) is implicated in many 11 navigation related processes. 12The CX of the insect brain is an unpaired, midline-spanning set of neuropils that consist of 13 the protocerebral bridge (PB), the ellipsoid body (also called lower division of the central body), 14 the fan-shaped body (also called upper division of the central body) and the paired noduli. These 15 neuropils and their characteristic internal organisation in vertical slices, combined with horizontal 16 1 layers are highly conserved across insects. This regular neuroarchitecture is generated by sets of 17 columnar cells, innervating individual slices, as well as large tangential neurons, innervating entire 18 layers. The structured projection patterns of columnar cells result in the PB being organised in 16 19 or 18 contiguous glomeruli and the ellipsoid body (EB) in 8 adjoined tiles. 20Crucially, the CX is of key importance for the computations required to derive a heading 21 signal [2,6,[11][12][13][14]. In locusts (Schistocerca gregaria), intracellular recordings have revealed a 22 neuronal layout that topographically maps the animal's orientation relative to simulated skylight 23 cues, including polarized light and point sources of light [15][16][17]. Calcium imaging of columnar 24 neurons connecting the EB and the PB (E-PG neurons) in the fruit fly Drosophila melanogaster, 25 revealed that the E-PG neuronal ensemble maintains localised spiking activity -commonly called 26 an activity 'bump' -that moves from one group of neurons to the next as the animal rotates 27 with respect to its...

Tyrosine hydroxylase immunostaining in the central complex of dicondylian insects

“…Three major categories of neurons innervating the CX have been distinguished across different species: Tangential neurons innervate distinct layers within the CX and largely provide input to the CX, while columnar and pontine neurons partition the CX into 16–18 columns or segments, provide internal right–left integration between columns and subunits, and, in the case of columnar neurons, send output signals to adjacent brain areas (Hanesch et al, 1989; Hulse et al, 2020; Pfeiffer & Homberg, 2014; Wolff et al, 2015). Evidence from several species including Drosophila , desert locust, cockroach, and others indicates that the columnar organization constitutes a neural network signaling head direction and spatial orientation, based on sky compass signals, visual panorama, and internally generated cues (Heinze & Homberg, 2007; Pisokas et al, 2020; Seelig & Jayaraman, 2015; Varga & Ritzmann, 2016; Zittrell et al, 2020). Outputs from the CX control heading and steering maneuvers during flight (Shiozaki et al, 2020) and walking (Green et al, 2019; Martin et al, 2015; Triphan et al, 2010).…”

Neural Population Computing: Parallel Distributed Processing, the Basal Ganglia, and Evolution

“…The adaptive value of such a mechanism provides a robust explanation for its evolutionary conservation dating back at least to arthropods. Evidence of a neurological basis for attractor dynamics has recently been reported in Drosophila [37][38][39][40]. Dupre and Yuste [41] have provided evidence of population encoding (but not attractor neurodynamics) in Hydra vulgaris, a far more primitive invertebrate classed in the phylum Cnidaria, which includes jelly fish.…”

Towards a multi-level understanding in insect navigation

“…Multi-level models can also be of interest for predicting how differences in neural connectivity between species may explain respective behavioural optimisations to their ecological needs [55]. For example [80] show how slight differences in the Central Complex connectivity between locusts and fruit flies, and may gift the first with a compass more resilient to noise (i.e. suitable for long-distance migration) and the second with a compass that is faster in responding to changes in direction (i.e.…”