How the insect central complex could coordinate multimodal navigation

Abstract

The central complex of the insect midbrain is thought to coordinate insect guidance strategies. Computational models can account for specific behaviours but their applicability across sensory and task domains remains untested. Here we assess the capacity of our previous model (Sun et al., 2020) of visual navigation to generalise to olfactory navigation and its coordination with other guidance in flies and ants. We show that fundamental to this capacity is the use of a biologically-plausible neural copy-and-shift mechanism that ensures sensory information is presented in a format compatible with the insect steering circuit regardless of its source. Moreover, the same mechanism is shown to allow the transfer cues from unstable/egocentric to stable/geocentric frames of reference providing a first account of the mechanism by which foraging insects robustly recover from environmental disturbances. We propose that these circuits can be flexibly repurposed by different insect navigators to address their unique ecological needs.

Transforming a head direction signal into a goal-oriented steering command

“…1c). This "copy-and-shift" architecture 21 is reminiscent of the design of a resolver servomotor (Extended Data Fig. 2).…”

A neural circuit for wind-guided olfactory navigation

“…Numerous studies have explored the role of the FB in path integration 31 , 33 visual navigation 34 and landmark-guided long-distance dispersal 35 – 37 . However, few studies have investigated the role of this region in olfactory navigation 38 .…”

Geometry-based navigation in the dark: Layout symmetry facilitates spatial learning in the house cricket,Acheta domesticus, in the absence of visual cues

“…Such possible information processing could be executed by the central complex as was proposed by Xuelong Sun et al's (2021) model. The central complex receives projections from antennal lobes, which are known to process, aside from chemosensory information, also the tactile stimuli (Nishino et al 2005).…”

“…On the contrary, crickets in the wild have to navigate in much more complex environments than simple testing arenas. However, in natural environments, they are constantly provided with information from more than one modality, and some results suggest that multimodal information may facilitate spatial learning (Taevs et al 2010; Hebets et al 2014; Buehlmann et al 2020; Sun et al 2021). Such possible information processing could be executed by the central complex as was proposed by Xuelong Sun et al’s (2021) model.…”