Rapid Aversive and Memory Trace Learning during Route Navigation in Desert Ants

Wystrach, Antoine; Buehlmann, Cornelia; Schwarz, Sebastian; Chen, Ken; Graham, Paul

doi:10.1016/j.cub.2020.02.082

Cited by 56 publications

(81 citation statements)

References 46 publications

(54 reference statements)

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“…Views facing the nest may as well be included during learning and categorised as left, right or both, explaining why most ants facing their goal usually choose to turn in one particular Revisiting current questions in insect and robot navigation such as early exploration, route following and homing 20,[46][47][48][49] ; the integration of aversive memories 8,24,50 , path integration and views ( [51][52][53][54] or other sensory modalities ( 55-58 as well as seeking for underlying neural correlates [5][6][7] -with such a lateralised design as a framework promises an interesting research agenda.…”

Section: Discussionmentioning

confidence: 99%

A lateralised design for the interaction of visual memories and heading representations in navigating ants

Wystrach¹,

Moël²,

Clément³

et al. 2020

Preprint

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The navigational skills of ants, bees and wasps represent one of the most baffling examples of the powers of minuscule brains. Insects store long-term memories of the visual scenes they experience, and they use compass cues to build a robust representation of directions. We know reasonably well how long-term memories are formed, in a brain area called the Mushroom Bodies (MB), as well as how heading representations are formed in another brain area called the Central Complex (CX). However, how such memories and heading representations interact to produce powerful navigational behaviours remains unclear. Here we combine behavioural experiments with computational modelling that is strictly based on connectomic data to provide a new perspective on how navigation might be orchestrated in these insects. Our results reveal a lateralised design, where signals about whether to turn left or right are segregated in the left and right hemispheres, respectively. Furthermore, we show that guidance is a two-stage process: the recognition of visual memories, presumably in the MBs, does not directly drive the motor command, but instead updates a desired heading, presumably in the CX, which in turn is used to control guidance using celestial compass information. Overall, this circuit enables ants to recognise views independently of their body orientation, and combines terrestrial and celestial cues in a way that produces exceptionally robust navigation.

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Section: Discussionmentioning

confidence: 99%

A lateralised design for the interaction of visual memories and heading representations in navigating ants

Wystrach¹,

Moël²,

Clément³

et al. 2020

Preprint

Self Cite

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show abstract

“…However, the addition of a negative reward (when the cue appears on the rear of the visual field) clearly corrects this problem ( figure 6B). This is of interest considering that insects are known to associate (innately or learned) positive or negative value to olfactory [40] and/or visual cues [2]. Even in the case of discrete filters, which did not carry any prior information of the cue's relative orientation, the model generates a consistent behaviour and coherent weight distribution for the E-PG to PFL3 synapses (figure 6C).…”

Section: A Memory To Modulate the Epg-pfl Connection Weightsmentioning

confidence: 99%

A unified mechanism for innate and learned visual landmark guidance in the insect central complex

Goulard

Buehlmann

Graham

et al. 2021

Preprint

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Insects can navigate efficiently in both novel and familiar environments, and this requires flexiblity in how they are guided by sensory cues. A prominent landmark, for example, can ellicit strong innate behaviours (attraction or menotaxis) but can also be used through learning as a specific directional cue to sustain navigation memory. However, the mechanisms that allow both pathways to co-exist, interact or override each other are largely unknown. Here we propose a model for behavioural integration based on the neuroanatomy of the central complex (CX) and adapted to control landmark guided behaviours. We consider a reward signal provided either by an innate attraction to landmarks or a long-term visual memory that modulates the formation of a local vector memory in the CX. Using an operant strategy for a simulated agent exploring a simple arena world with a single cue, we show how the short-term memory generated can support both innate and learned steering behaviour. In addition, we show how this architecture is consistent with observed effects of unilateral mushroom bodies (MB) lesions in ants that cause a reversion to innate behaviour. We suggest the formation of a directional memory in the CX can be interpreted as transforming rewarding (positive or negative) sensory signals into a geometrical attractiveness (or repulsion) mapping of the environment. We discuss how this scheme might represent an ideal way to combine multisensory information gathered during the exploration of an environment and support optimized cue integration.

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“…It is known that handling of insects induces stress and the release of neuromodulators, which can alter behaviour long after the cause of the stress has ceased (Davenport and Evans, 1984;Harris and Woodring, 1992;Roeder, 1999). A recent study has also shown how aversive experiences can quickly affect the behaviour of ants (Wystrach et al, 2020). The diminished need for manipulation of the animal also facilitates the transition between naturalistic fieldwork and a fully controlled laboratory approach.…”

Section: Advantages and Disadvantages Of The Motion Compensatormentioning

confidence: 99%

“…However, tethering will inevitably induce physical discrepancies in the sensorimotor control of behaviour (Paulk et al, 2015;Stowers et al, 2017), potentially affecting the quantitative identification of sensorimotor transformation(s) from the analyses of input-output relationships. In addition, the constant constraints applied, both by the tether and by the inherent manipulations to set it, can quickly induce aversive experiences and subsequently change the behaviour of ants engaged in a navigation task (Wystrach et al, 2020). It also reduces the ease of transferring animals between the real world and VR, e.g.…”

Section: Introductionmentioning

confidence: 99%

A motion compensation treadmill for untethered wood ants (Formica rufa): evidence for transfer of orientation memories from free-walking training

Goulard

Buehlmann

Graham

et al. 2020

Journal of Experimental Biology

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The natural scale of insect navigation during foraging makes it challenging to study under controlled conditions. Virtual reality and trackball setups have offered experimental control over visual environments while studying tethered insects, but potential limitations and confounds introduced by tethering motivates the development of alternative untethered solutions. In this paper, we validate the use of a motion compensator (or ‘treadmill’) to study visually driven behaviour of freely moving wood ants (Formica rufa). We show how this setup allows naturalistic walking behaviour and preserves foraging motivation over long time frames. Furthermore, we show that ants are able to transfer associative and navigational memories from classical maze and arena contexts to our treadmill. Thus, we demonstrate the possibility to study navigational behaviour over ecologically relevant durations (and virtual distances) in precisely controlled environments, bridging the gap between natural and highly controlled laboratory experiments.

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Rapid Aversive and Memory Trace Learning during Route Navigation in Desert Ants

Cited by 56 publications

References 46 publications

A lateralised design for the interaction of visual memories and heading representations in navigating ants

A lateralised design for the interaction of visual memories and heading representations in navigating ants

A unified mechanism for innate and learned visual landmark guidance in the insect central complex

A motion compensation treadmill for untethered wood ants (Formica rufa): evidence for transfer of orientation memories from free-walking training

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