Biology subjects

Wystrach, A.

Publications and source records attributed to Wystrach, A..

18 recordsLinked to original sources

bioRxiv2026

Predictive coding and oscillations underlie the optomotor response in distant insect lineages

The optomotor response (OMR) refers to animals distinctive turning response to rotating visual stimuli. It is assumed to be a predictable Stimulus-Response (S-R) behavior. Here we show in two phylogenetically and ecologically distant insects (ants and earwigs) that it is not the case. Insects turning responses were not determined by the detected visual-motion, but by the computation of optic flow prediction errors, which we could infer by manipulating the visual-feedback expected from their own movements. Moreover, both insects displayed regular oscillations of angular velocity, which were modulated by the prediction errors. This produces a closed-loop system yielding complex dynamics and a stochastic moment-to-moment behavior, which can be captured with a simple predictive computational model. We conclude that internal oscillators and predictive coding, as well as their closed-loop interaction, are ancestral features of insect brains conserved across more than 350 million years. The OMR is a by-product of this control system and appears deterministic only when averaging animals responses.

neuroscience↗

bioRxiv2026

Online extinction and novelty-triggered recovery of life-long visual memories in navigating ants

Insects exhibit flexible memory processes, yet current models often confine these modulations to discrete, reinforced events. During navigation, animals can learn to associate locations with resources or aversive events. However, such events occur sporadically within an otherwise continuous behavioral process involving latent learning. This raises a fundamental question for insect cognition: can insects continuously update visual memories during navigation? We show that navigating ants (Myrmecia midas) dynamically revalue visual memories en-route, even in the absence of any motivational change or external reinforcement. Using a trackball system that prevented visual progress, we found that nest-view attraction declined over time, reflecting a gradual, online extinction of these otherwise life-long attractive visual memories. These memory updates were view-specific, independent of path integrator state, and persisted after 24-hours, indicating the involvement of long-term memory processes. However, brief exposure to a novel visual scene was sufficient to partially restore nest-views attraction, showing that extinction is labile, and the original memories are preserved. Unlike classic paradigms, visual memory extinction operates here as a continuous, time-dependent process without reward-omission or prediction error; whereas memory reinstatement is triggered by discrete visual changes. We propose that these dynamics are mediated by opponent-processes in the insect mushroom bodies, where temporal estimates of view exposure drive extinction and novel view detection gates memory recovery.

ecology↗

bioRxiv2025

Scanning and active sampling behaviours emerge from conserved insect neural circuits

Navigating insects often pause and rotate to sample their surroundings, behaviours termed scanning. These and other active sampling behaviours embody navigational uncertainty, and are key for spatial learning, yet their neural basis remains unclear and existing models impose scanning behaviours rather than explaining its emergence. Here, we show that desert ants scanning dynamics can emerge spontaneously from the same conserved neural circuits used for goal-directed navigation, without requiring a specialized scanning module. We built a biologically grounded model combining central complex (CX) steering and lateral accessory lobe (LAL) oscillators, and added a downstream stochastic inhibition of forward speed. This minimal system produced diverse, realistic scan dynamics; saccades, fixations and reversals, whose features were qualitatively compared to high-speed video recordings of Melophorus bagoti scanning. Detailed analysis of these natural scans confirmed model predictions, including how scan structure depends on oscillator phase, goal-heading deviation, and navigational uncertainty. Furthermore, the model reveals that simple modulation of forward speed unifies a broad range of behaviours across ant species, from dashes to smooth oscillatory trajectories to pirouettes and voltes. Crucially, this model suggests a distributed control principle where forward speed acts as a single adjustable parameter, for both individuals and through evolution, to regulate the balance between goal-driven exploitation and information-seeking exploration.

animal behavior and cognition↗

bioRxiv2024

A comparative study of navigation behaviours in ants

Ants inhabit a vast range of ecosystems and exhibit wide morphology. They are expert navigators employing a handful of well-understood navigational strategies. However, the specific relationships among ant navigation behaviours, ecology, and morphology remain unclear, highlighting the need for comparative studies across diverse species. Here, we conducted field displacement experiments with 15 ant species across different habitats, assessing the prevalence of path integration, view-based navigation, olfactory trail following, and backtracking. We further tested whether use of particular navigation strategies was correlated with variation in morphological traits that could affect navigation efficiency, namely body size, eye size (view-based, path integration) and scape length (olfactory). There was a negative correlation between path integration and olfaction across different ant species, and no other clear trade-offs were identified between navigational strategies. Olfactory navigation emerged as the most dominant strategy. Path integration was also prevalent but limited to arboreal ants. View-based navigation was observed in both ground-foraging and tree-climbing ant species, and, unexpectedly, backtracking was also widespread. Species with larger eyes and body size showed a stronger preference for view-based navigation. However, no significant relationship was found between eye size or antennal scape length with preference for either path integration or olfaction. These results highlight the diversity and specialization of navigational strategies in ants, which appear to depend on the species ecological niche and morphological traits. Our study confirmed that path integration performs better in open sky environments, while view-based navigation appears more effective in cluttered habitats. We also showed the importance of plasticity in both foraging strategies and navigational profile at individual and colony levels, demonstrating the adaptability of ants navigation strategies to their environment.

ecology↗

bioRxiv2024

Vision is not olfaction: impact on the insect Mushroom Bodies connectivity

The Mushroom Bodies, a prominent and evolutionary conserved structure of the insect brain, are known to be the support of olfactory memory. There is now evidence that this structure is also required for visual learning, but the hypotheses about how the view memories are encoded are still largely based on what is known of the encoding of olfactory information. The different processing steps happening along the several relays before the Mushroom Bodies is still unclear, and how the visual memories actually may allow navigation is entirely unknown. Existing models of visual learning in the Mushroom Bodies quickly fall short when used in a navigational context. We discuss how the visual world differs from the olfactory world and what processing steps are likely needed in order to form memories useful for navigation, and demonstrate it using a computational model of the Mushroom Bodies embedded in an agent moving in through a virtual 3D world.

animal behavior and cognition↗

bioRxiv2024

Latent learning without map-like representation of space in navigating ants

Desert ants are excellent navigators. Each individual learns long foraging routes meandering between the trees and bushes in their natural habitat. It is well-known how the insect brain memorizes and recognizes views, and how this recognition can guide their way. However, little is known about the rule that guide spatial learning in the first place. Here we recorded the paths of desert ants navigating in their natural habitat under various displacement conditions. We demonstrate that ants learn continuously the routes they travel and memorize them in one trial, without the need for reward or punishment, and even if these routes are meandering and do not lead to places of interest: a concept called latent learning, which is typically associated with the formation of map-like representation in vertebrates. Yet, the failure of ants to solve simple artificial navigation tasks -even with the goal being clearly visible- reveals that they relied on egocentric visual memories without map-like representation of the surrounding space. Our results unveil the rules governing the formation and recall of latent memories. A model shows that it can be implemented in the insects Mushroom bodies brain area through dynamic interactions between short- and long-lasting memories.

animal behavior and cognition↗

bioRxiv2024

Is this scenery worth exploring? Insight into the visual encoding of navigating ants.

Solitary foraging insects like desert ants rely heavily on vision for navigation. While ants can learn visual scenes, it is unclear what cues they use to decide if a scene is worth exploring at the first place. To investigate this, we recorded the motor behavior of Cataglyphis velox ants navigating in a virtual reality set-up and measured their lateral oscillations in response to various unfamiliar visual scenes under both closed-loop and open-loop conditions. In naturalistic-looking panorama, ants display regular oscillations as observed outdoors, allowing them to efficiently scan the scenery. Manipulations of the virtual environment revealed distinct functions served by dynamic and static cues. Dynamic cues, mainly rotational optic flow, regulated the amplitude of oscillations but not their regularity. Conversely, static cues had little impact on the amplitude but were essential for producing regular oscillations. Regularity of oscillations decreased in scenes with only horizontal, only vertical or no edges but was restored in scenes with both edge types together. The actual number of edges, the visual pattern heterogeneity across azimuths, the light intensity or the relative elevation of brighter regions did not affect oscillations. We conclude that ants use a simple but functional heuristic to determine if the visual world is worth exploring, relying on the presence of at least two different edge orientations in the scene. Summary statementUsing a virtual reality setup, we reveal that ants rely on a heuristic to trigger visual exploration in an unfamiliar scene. The simultaneous presence of vertical and horizontal edges is necessary and sufficient for the ants to produce lateral oscillations and scan the scene.

animal behavior and cognition↗

bioRxiv2023

Smell and Aftersmell: Fast Calcium Imaging Dynamics of Honey Bee Olfactory Coding

Odour processing exhibits multiple parallels between vertebrate and invertebrate olfactory systems. Insects, in particular, have emerged as relevant models for olfactory studies because of the tractability of their olfactory circuits. Here, we used fast calcium imaging to track the activity of projection neurons in the honey bee antennal lobe (AL) during olfactory stimulation at high temporal resolution. We observed a heterogeneity of response profiles and an abundance of inhibitory activities, resulting in various response latencies and stimulus- specific post-odour neural signatures. Recorded calcium signals were fed to a mushroom body (MB) model constructed implementing the fundamental features of connectivity between olfactory projection neurons, Kenyon cells (KC), and MB output neurons (MBON). The model accounts for the increase of odorant discrimination in the MB compared to the AL and reveals the recruitment of two distinct KC populations that represent odorants and their aftersmell as two separate but temporally coherent neural objects. Finally, we showed that the learning- induced modulation of KC-to-MBON synapses can explain both the variations in associative learning scores across different conditioning protocols used in bees and the bees response latency. Thus, it provides a simple explanation of how the time contingency between the stimulus and the reward can be encoded without the need for time tracking. This study broadens our understanding of olfactory coding and learning in honey bees. It demonstrates that a model based on simple MB connectivity rules and fed with real physiological data can explain fundamental aspects of odour processing and associative learning.

neuroscience↗

bioRxiv2023

Ants integrate proprioception, visual context and efference copies to make robust predictions.

Feedforward models are mechanisms enabling an agent to predict the sensory outcomes of its actions. It can be implemented in the nervous system in the form of efference copies, which are copies of motor signals that are subtracted from the sensory stimulation actually detected, literally cancelling the perceptual outcome of the predicted action. In insects, efference copies are known to modulate optic flow detection for flight control in fruit flies. Much less is known, however, about possible feedforward control in other insects. Here we investigated whether feedforward control occurs in the detection of horizontal optic flow in walking ants, and how the latter is integrated to modulate their locomotion. We mounted Cataglyphis velox ants within a virtual reality set-up, allowing us to manipulate the relationship between the ants movements and the optic flow it perceives. Results show that ants do compute a prediction error by making the difference between the expected optic flow according to their own movements and the one it perceived. Interestingly, this prediction does not control locomotion directly, but modulates the ants intrinsic oscillator, which produces continuous alternations between right and left turns. Whats more, we show that the prediction also involves proprioceptive feedback, and is additionally modulated by the visual structure of the surrounding panorama in a functional way. Finally, prediction errors stemming from both eyes are integrated before modulating the oscillator, providing redundancy and robustness to the system. Overall, our study reveals that ants compute robust predictions of the optic flow they should receive using a distributed mechanism integrating feedforwards, feedbacks as well as innate information about the structure of the world, that control their locomotion through oscillations.

animal behavior and cognition↗

bioRxiv2023

Neurons from pre-motor areas to the Mushroom bodies can orchestrate latent visual learning in navigating insects.

Spatial learning is peculiar. It can occur continuously and stimuli of the world need to be encoded according to some spatial organisation. Recent evidence showed that insects categorise visual memories as whether their gaze is facing left vs. right from their goal, but how such categorisation is achieved during learning remains unknown. Here we analysed the movements of ants exploring the world around their nest, and used a biologically constrained neural model to show that such parallel, lateralized visual memories can be acquired straightforwardly and continuously as the agent explore the world. During learning, left and right visual memories can be formed in different neural comportments (of the mushroom bodies lobes) through existing lateralised dopaminergic neural feedback from pre-motor areas (the lateral accessory lobes) receiving output from path integration (in the central complex). As a result, path integration organises visual learning internally, without the need to be expressed through behaviour; and therefore, views can be learnt continuously (without suffering memory overload) while the insect is free to explore the world randomly or using any other navigational mechanism. After learning, this circuit produces robust homing performance in a 3D reconstructed natural habitat despite a noisy visual recognition performance. Overall this illustrates how continuous bidirectional relationships between pre-motor areas and visual memory centres can orchestrate latent spatial learning and produce efficient navigation behaviour.

neuroscience↗

bioRxiv2023

Compensation to visual impairments and behavioral plasticity in navigating ants

Desert ants are known to rely heavily on vision while venturing for food and returning to the nest. During these foraging trips, ants memorize and recognize their visual surroundings, which enables them to recapitulate individually learnt routes in a fast and effective manner. The compound eyes are crucial for such visual navigation; however, it remains unclear how information from both eyes are integrated and how ants cope with visual impairment. Here we manipulated the ants visual system by covering one of the two compound eyes and analyzed their ability to recognize familiar views in various situations. Monocular ants showed an immediate disruption of their ability to recapitulate their familiar route. However, they were able to compensate for the visual impairment in a few hours by restarting a route-learning ontogeny, as naive ants do. This re-learning process with one eye forms novel memories, without erasing the previous memories acquired with two eyes. Additionally, ants having learnt a route with one eye only are unable to recognize it with two eyes, even though more information is available. Together, this shows that visual memories are encoded and recalled in an egocentric and fundamentally binocular way, where the visual input as a whole must be matched to enable recognition. We show how this kind of visual processing fits with their neural circuitry. Significance StatementIf humans look at the world with both eyes, they have no problem to then recognize it with one eye only, and vice-versa. Thus, our way of encoding the world is robust to changes of the visual field. Yet ants do so very differently. Views learnt with two eyes can only be recognized with two eyes, and views learnt with one eye can only be recognized with one eyes (the same eye). However, this rigidity is compensated by a remarkable behavioral flexibility. Upon covering one eye, ants - which can no longer recognize their familiar surroundings - will restart a learning process to store these novel visual inputs in a parallel memory and resume their normal foraging activity.

animal behavior and cognition↗

bioRxiv2022

An intrinsic oscillator underlies visual navigation in ants.

Controlling behavior implies a constant balance between exploration - to gather information - and exploitation - to use this information to reach ones goal. However, how this tradeoff is achieved in navigating animals is unclear. Here we recorded the paths of two phylogenetically distant visually navigating ant species (Myrmecia croslandi and Iridomyrmex purpureus) using a trackball-treadmill directly in their habitat. We show that both species continuously produce regular lateral oscillations with bursts of forward movement when facing the general direction of travel, providing a remarkable tradeoff between visual exploration across directions and movement areas. This dynamical signature is conserved across navigational contexts but requires certain visual cues to be fully expressed. Rotational feedback regulates the extent of turns, but is not required to produce them, indicating that oscillations are generated intrinsically. Learnt visual information modulates the oscillations amplitudes to fit the task at hand in a continuous manner: an unfamiliar panorama enhances the amplitude of oscillations in both naive and experienced ants, favoring visual exploration; while a learnt familiar panorama reduces them, favoring exploitation through. The observed dynamical signature readily emerges from a simple neural-circuit model of the insects conserved pre-motor area known as the lateral accessory lobe, endorsing oscillations as a core, ancestral way of moving in insects. We discuss the importance and evolution of self-generated behaviors and how such an oscillator has been exapted to various modalities, behaviors and way of moving.

animal behavior and cognition↗

bioRxiv2021

Aversive View Memory and Navigational Risk Sensitivity in the Desert Ant, Cataglyphis Velox

Many ants establish foraging routes through learning views of the visual panorama. Route models have focused primarily on attractive view use, which experienced foragers orient towards to return to known sites. However, aversive views have recently been uncovered as a key component of route learning. Here, Cataglyphis velox rapidly learned aversive views, when associated with a negative outcome, a period of captivity in brush, triggering an increase in hesitation behavior. These memories were based on the accumulation of experiences over multiple trips with each new experience regulating foragers hesitancy. Foragers were also sensitive to captivity time differences, suggesting they possess some mechanism to quantify duration. Finally, we analyzed foragers perception of risky (i.e. variable) versus stable aversive outcomes by associating two sites along the route with distinct captivity schedules, a fixed or variable duration, with the same mean across training. Foragers exhibited significantly less hesitation to the risky outcome compared to the fixed, indicating they perceived risky outcomes as less severe. Results align with a logarithmic relationship between captivity duration and hesitations, suggesting that aversive stimulus perception is a logarithm of its actual value. We conclude by characterizing how these behaviors can be executed within the mushroom bodies neural circuitry.

animal behavior and cognition↗

bioRxiv2020

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

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 1, and they use compass cues to build a robust representation of directions 2,3. We know reasonably well how long-term memories are formed, in a brain area called the Mushroom Bodies (MB) 4-8, as well as how heading representations are formed in another brain area called the Central Complex (CX) 9-12. However, how such memories and heading representations interact to produce powerful navigational behaviours remains unclear 7,13,14. 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.

animal behavior and cognition↗

bioRxiv2019

How do backward walking ants (Cataglyphis velox) cope with navigational uncertainty?

Current opinion in insect navigation assumes that animals need to align with the goal direction to recognise familiar views and approach it. Yet, ants sometimes drag heavy food items backward to the nest and it is still unclear to what extent they rely on visual memories while doing so. In this study displacement experiments and alterations of the visual scenery reveal that ants do indeed recognise and use the learnt visual scenery to guide their path while walking backward. In addition, the results show that backward homing ants estimate their directional certainty by combining visual familiarity with other cues such as their path integrator and the time spent backward. A simple model that combines path integration with repulsive and attractive visual memories captures the results.

animal behavior and cognition↗

bioRxiv2019

Opponent processes in visual memories: a model of attraction and repulsion in navigating insects' mushroom bodies.

Solitary foraging insects display stunning navigational behaviours in visually complex natural environments. Current literature assumes that these insects are mostly driven by attractive visual memories, which are learnt when the insects gaze is precisely oriented toward the goal direction, typically along its familiar route or towards its nest. That way, an insect could return home by simply moving in the direction that appears most familiar. Here we show using virtual reconstructions of natural environments that this principle suffers from fundamental drawbacks, notably, a given view of the world does not provide information about whether the agent should turn or not to reach its goal. We propose a simple model where the agent continuously compares its current view with both goal and anti-goal visual memories, which are treated as attractive and repulsive respectively. We show that this strategy effectively results in an opponent process, albeit not at the perceptual level - such as those proposed for colour vision or polarisation detection - but at the level of environmental space. This opponent process results in a signal that strongly correlates with the angular error of the current body orientation so that a single view of the world now suffices to indicate whether the agent should turn or not. By incorporating this principle into a simple agent navigating in reconstructed natural environments, we show that it overcomes the usual shortcomings and produces a step-increase in navigation effectiveness and robustness. Our findings provide a functional explanation to recent behavioural observations in ants and why and how so-called aversive and appetitive memories must be combined. We propose a likely neural implementation based on the insect mushroom bodies circuitry that produces behavioural and neural predictions contrasting with previous models. Author summaryInsects such as ants and bees are excellent navigators, able to learn long foraging routes and return to their nest in complex natural habitats. To achieve this, it is believed that individuals memorise views - the visual scene as they perceive it - only when their body is precisely oriented towards the goal. As a result, the insect can return to its goal by simply being attracted in the direction that represents the highest visual familiarity. Here we use a computational approach to show that this strategy suffers from a major weakness: a single view of the world does not suffice to tell whether the agent should turn or not to reach its goal. However, a surprisingly robust solution to this problem arises if we simply assume that these insects memorise not only goal-oriented views but also anti-goal-oriented views that they then treat as repulsive. This idea clarifies several observed behaviours that were difficult to explain with previous models. Overall, this research helps us to understand how insects combine memories in specific brain areas and can navigate so efficiently despite their tiny brain.

animal behavior and cognition↗

bioRxiv2019

Avoiding pitfalls: Trace conditioning and rapid aversive learning during route navigation in desert ants

The ability of bees and ants to learn long visually guided routes in complex environments is perhaps one of the most spectacular pieces of evidence for the impressive power of their small brains. While flying bees can visit flowers in an optimised sequence over kilometres, walking ants can precisely recapitulate routes of up to a hundred metres in complex environments. It is clear that route following depends largely on learnt visual information and we have good idea how views can guide individuals along them, however little is known about the mechanisms that control route learning and development. Here we show that ants in natural environments can actively learn a route detour to avoid a pit trap and that this depends on a process analogous to aversive trace conditioning. Views experienced before falling into the trap become associated with the ensuing negative outcome and thus trigger salutary turns on the subsequent trip. This drives the ants to orient away from the goal direction and avoid the trap. If the pit is avoided, the novel views experienced during the detour become positively reinforced and the new route crystallises. We discuss how such an interplay between appetitive and aversive memories might be implemented in insect neural circuitry.

animal behavior and cognition↗

bioRxiv2019

Intrinsic control of muscle attachment sites matching

How a stereotypic muscle pattern is established, and adapted to fit locomotion behaviour is a fascinating question. Here we set up the targeted deletion of cis-regulatory modules (CRMs) controlling the transcription of Drosophila muscle identity transcription factors (iTF) to generate larval muscle identity mutants. By focusing on one muscle transcription and morphology, we show that selection of muscle attachment sites and the precision of muscle/muscle matching is intrinsic to muscle identity. It involves propagation of the iTF expression code from a founder myoblast to the other syncytial nuclei after fusion. Live imaging indicates that the precise staggered muscle attachment pattern involves attraction to tendon cells and homotypic repulsion. Unbalance leads to the formation of abnormal, branched muscles. Single muscle morphology shifts induce subtle locomotor behaviour. Together this work highlights that CRM deletion is an effective setting for creating muscle-specific defects and branched muscles, as new paradigms to study the development of human myopathies affecting subsets of muscles. Highlights- First muscle-identity mutants, via deletion of specific cis-regulatory modules - Reprogramming of syncytial nuclei is key to muscle morphological identity - Selection of muscle attachment sites; attraction and retraction intrinsic to muscle identity - Genetically controlled formation of branched muscles, a new paradigm for functional studies - Single muscle morphology shift induces subtle locomotor behaviour modification

developmental biology↗