Path integration: how details of the honeybee waggle dance and the foraging strategies of desert ants might help in understanding its mechanisms

Abstract

Path integration is a navigational strategy that gives an animal an estimate of its position relative to some starting point. For many decades, ingenious and probing behavioural experiments have been the only window onto the operation of path integration in arthropods. New methods have now made it possible to visualise the activity of neural circuits in Drosophila while they fly or walk in virtual reality. Studies of this kind, as well as electrophysiological recordings from single neurons in the brains of other insects, are revealing details of the neural mechanisms that control an insect's direction of travel and other aspects of path integration. The aim here is first to review the major features of path integration in foraging desert ants and honeybees, the current champion path integrators of the insect world, and second consider how the elaborate behaviour of these insects might be accommodated within the framework of the newly understood neural circuits. The discussion focuses particularly on the ability of ants and honeybees to use a celestial compass to give direction in Earth-based coordinates, and of honeybees to use a landscape panorama to provide directional guidance for path integration. The possibility is raised that well-ordered behaviour might in some cases substitute for complex circuitry. A 5 min Activation Distance from centre (cm) 0 3 6 B C 10 cm REVIEW

Multimodal interactions in insect navigation

“…One widespread innate navigational strategy is path integration (PI), where ants keep track of direction (Wehner and Mueller 2006) and distance travelled (Wittlinger et al 2006) and continually integrate this information such that they can travel directly to their nest from any point during a foraging journey (Wehner and Srinivasan 2003;Ronacher 2008;Collett 2019). This innate strategy allows ants to explore the environment while being safely connected to the nest and, furthermore, gives foragers the chance to learn relevant environmental cues about locations and foraging routes.…”

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

“…Central-place foraging insects navigate using a ‘toolkit’ of independent guidance systems ( Wehner, 2009 ) of which the most fundamental are path integration (PI), whereby foragers track the distance and direction to their nest by integrating the series of directions and distances travelled (for reviews see Heinze et al, 2018 ; Collett, 2019 ), and visual memory (VM), whereby foragers derive a homing signal by comparing the difference between current and stored views (for reviews see Zeil, 2012 ; Collett et al, 2013 ). Neurophysiological and computational modelling studies advocate the central complex neuropil (CX) as the PI centre ( Heinze and Homberg, 2007 ; Seelig and Jayaraman, 2015 ; Stone et al, 2017 ), whereas the mushroom body neuropils (MB) appear well suited to assessing visual valence as needed for VM ( Heisenberg, 2003 ; Ardin et al, 2016 ; Müller et al, 2018 ).…”

Dynamic multimodal interactions in navigating wood ants: What do path details tell us about cue integration?

“…Ants are remarkable navigators, with their efficiency coming from the coordinated implementation of a set of navigational strategies (Wehner, 2003;Collett et al, 2013;Knaden and Graham, 2016). Some ant species utilise their social nature and develop pheromone trail networks to recruit ants between the nest and reliable food locations (Czaczkes et al, 2015), while others forage individually and rely on path integration (PI) to explore the environment while being safely connected to the nest (Heinze et al, 2018;Collett, 2019). As these solitary forager ants become familiar with a terrain, visual and olfactory information from the environment is learnt to enable them to navigate along routes (visual: Collett et al, 1992;Kohler and Wehner, 2005;Graham and Collett, 2006;Wystrach et al, 2011;Mangan and Webb, 2012;olfactory: Buehlmann et al, 2015) and locate the nest (visual: Wehner and Räber, 1979;Wehner et al, 1996;Narendra et al, 2007;olfactory: Steck, 2012) or a familiar feeder (visual: Durier et al, 2003;Collett et al, 2014;Buehlmann et al, 2016;olfactory: Huber and Knaden, 2018).…”