Mushroom Bodies Are Required for Learned Visual Navigation, but Not for Innate Visual Behavior, in Ants

Buehlmann, Cornelia; Wozniak, Beata; Goulard, Roman; Webb, Barbara; Graham, Paul

doi:10.1016/j.cub.2020.07.013

Cited by 88 publications

(116 citation statements)

References 40 publications

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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

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show abstract

“…The approach uses a known anatomical shift between functional columns that exists in the CX to build a memory of the relationship between self-motion and the compass signal, following a similar principle to the path integrator described in [19]. Modulating a synaptic memory formation under the control of external sensory inputs that provide reward information, we showed how this architecture was able to drive oriented behaviour; mimicking both innate attraction to a bar [7; 10] and reaching a memorized location [11]. Such a memory process is coherent with the CX central role in spatial learning [45] as well as the storage of short-term orientation memory [46].…”

Section: Discussionmentioning

confidence: 99%

“…In order to link our model to biological experiments [11], we set up simulations where the MB could be silenced completely. The first step was to duplicate the MB used in previous simulation to obtain two bilateral identical structures.…”

Section: Lesion Experimentsmentioning

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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“…CO 2 signaling is modestly involved in sensory learning. The calyces of the mushroom bodies are a neuropil for sensory integration and memory, important for experience-dependent reactions [51][52][53][54][55] . In contrast to the main olfactory pathway, which innervates the Ca extensively (Fig.…”

Section: Discussionmentioning

confidence: 99%

Neuronal architecture of the second-order CO2 pathway in the brain of a noctuid moth

Chu

Ian

et al. 2020

Sci Rep

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Many insects possess the ability to detect fine fluctuations in the environmental CO2 concentration. In herbivorous species, plant-emitted CO2, in combination with other sensory cues, affect many behaviors including foraging and oviposition. In contrast to the comprehensive knowledge obtained on the insect olfactory pathway in recent years, we still know little about the central CO2 system. By utilizing intracellular labeling and mass staining, we report the neuroanatomy of projection neurons connected with the CO2 sensitive antennal-lobe glomerulus, the labial pit organ glomerulus (LPOG), in the noctuid moth, Helicoverpa armigera. We identified 15 individual LPOG projection neurons passing along different tracts. Most of these uniglomerular neurons terminated in the lateral horn, a previously well-described target area of plant-odor projection neurons originating from the numerous ordinary antennal-lobe glomeruli. The other higher-order processing area for odor information, the calyces, on the other hand, was weakly innervated by the LPOG neurons. The overlapping LPOG terminals in the lateral horn, which is considered important for innate behavior in insects, suggests the biological importance of integrating the CO2 input with plant odor information while the weak innervation of the calyces indicates the insignificance of this ubiquitous cue for learning mechanisms.

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Mushroom Bodies Are Required for Learned Visual Navigation, but Not for Innate Visual Behavior, in Ants

Cited by 88 publications

References 40 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

Neuronal architecture of the second-order CO2 pathway in the brain of a noctuid moth

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