A decentralised neural model explaining optimal integration of navigational strategies in insects

Abstract

Insect navigation arises from the coordinated action of concurrent guidance systems but the neural mechanisms through which each functions, and are then coordinated, remains unknown. We propose that insects require distinct strategies to retrace familiar routes (route-following) and directly return from novel to familiar terrain (homing) using different aspects of frequency encoded views that are processed in different neural pathways. We also demonstrate how the Central Complex and Mushroom Bodies regions of the insect brain may work in tandem to coordinate the directional output of different guidance cues through a contextually switched ring-attractor inspired by neural recordings. The resultant unified model of insect navigation reproduces behavioural data from a series of cue conflict experiments in realistic animal environments and offers testable hypotheses of where and how insects process visual cues, utilise the different information that they provide and coordinate their outputs to achieve the adaptive behaviours observed in the wild.

The connectome of the adultDrosophilamushroom body: implications for function

“…A role for the MB in guiding locomotion and navigation in ants and other insects has been proposed (Ardin et al, 2016;Collett and Collett, 2018;Kamhi et al, 2020;Kim et al, 2019;Mizunami et al, 1998; Le Möel F, Wystrach A. 2020; Paulk and Gronenberg, 2008;Sun et al, 2020). The strong and direct connections we observed from the majority of MBONs to the CX, the fly's navigation and locomotion control center, provide one circuit path for the MB to exert influence on motor behaviors.…”

The connectome of the adult Drosophila mushroom body provides insights into function

“…A role for the MB in guiding locomotion and navigation in ants and other insects has been proposed ( Ardin et al, 2016 ; Collett and Collett, 2018 ; Kamhi et al, 2020 ; Kim et al, 2019 ; Mizunami et al, 1998 ; Le Möel and Wystrach, 2020 ; Paulk and Gronenberg, 2008 ; Sun et al, 2020 ). The strong and direct connections we observed from the majority of MBONs to the CX, the fly’s navigation and locomotion control center, provide one circuit path for the MB to exert influence on motor behaviors.…”

The Critical Role of Head Movements for Spatial Representation During Bumblebees Learning Flight

“…To return home, these insects have been shown to use a variety of strategies. For example, they can use path integration (PI) and view matching (Wehner, 2009 ; Zeil, 2012 ; Webb, 2019 ; Sun et al, 2020 ). PI gives them knowledge about their position relative to their nest-hole (Muller and Wehner, 1988 ; Wehner et al, 1996 ).…”

“…However, this egocentered information might be uncertain in the nest vicinity (Cheung et al, 2007 ; Cheung and Vickerstaff, 2010 ; Wystrach et al, 2015 ; Hoinville and Wehner, 2018 ; Webb, 2019 ). Therefore, insects also rely on view-matching in the final approach to their nest (Zeil, 2012 ; Webb, 2019 ; Sun et al, 2020 ). An insect is thought to compare its current retinotopic representation of the environment with one or several previously-stored views of its nest surroundings (Doussot et al, 2020a ).…”