Learning by your bootstraps
Navigation involves a plethora of sensory modalities, some of which are useful for naive animals and some of which involve learning. Previously, Pauline Fleischmann and colleagues demonstrated the really exciting result that naive ants use the magnetic field to “bootstrap” the learning walks by which they learn visual information. They now show that when experienced ants are “re-learning” visual information they don’t primarily rely on the magnetic field, although the information is still present. Presumably they can “bootstrap” their new learning walks using the celestial compass information that they learnt as naive ants.
Abstract: “At the beginning of their foraging careers, Cataglyphis desert ants calibrate their compass systems and learn the visual panorama surrounding the nest entrance. For that, they perform well-structured initial learning walks. During rotational body movements (pirouettes), naïve ants (novices) gaze back to the nest entrance to memorize their way back to the nest. To align their gaze directions, they rely on the geomagnetic field as a compass cue. In contrast, experienced ants (foragers) use celestial compass cues for path integration during food search. If the panorama at the nest entrance is changed, foragers perform re-learning walks prior to heading out on new foraging excursions. Here, we show that initial learning walks and re-learning walks are structurally different. During re-learning walks, foragers circle around the nest entrance before leaving the nest area to search for food. During pirouettes, they do not gaze back to the nest entrance. In addition, foragers do not use the magnetic field as a compass cue to align their gaze directions during re-learning walk pirouettes. Nevertheless, magnetic alterations during re-learning walks under manipulated panoramic conditions induce changes in nest-directed views indicating that foragers are still magnetosensitive in a cue conflict situation.”
Fleischmann, P.N., Grob, R. & Rössler, W. Magnetosensation during re-learning walks in desert ants (Cataglyphis nodus). J Comp Physiol A (2021).
Choosing the middle of the banquet
We often think about Path Integration as being a mechanism for returning to a discrete target location. However, in real world foraging situations animals are faced with a range of food locations which have to be mapped onto a single coordinate for a PI mechanism. Behbahani et al show that flies map multiple locations onto a single PI location.
Abstract: “The ability to keep track of one’s location in space is a critical behavior for animals navigating to and from a salient location, and its computational basis is now beginning to be unraveled. Here, we tracked flies in a ring-shaped channel as they executed bouts of search triggered by optogenetic activation of sugar receptors. Unlike experiments in open field arenas, which produce highly tortuous search trajectories, our geometrically constrained paradigm enabled us to monitor flies’ decisions to move toward or away from the fictive food. Our results suggest that flies use path integration to remember the location of a food site even after it has disappeared, and flies can remember the location of a former food site even after walking around the arena one or more times. To determine the behavioral algorithms underlying Drosophila search, we developed multiple state transition models and found that flies likely accomplish path integration by combining odometry and compass navigation to keep track of their position relative to the fictive food. Our results indicate that whereas flies re-zero their path integrator at food when only one feeding site is present, they adjust their path integrator to a central location between sites when experiencing food at two or more locations. Together, this work provides a simple experimental paradigm and theoretical framework to advance investigations of the neural basis of path integration.”
Behbahani, A. H., Palmer, E. H., Corfas, R. A. & Dickinson, M. H. 2021 Drosophila re-zero their path integrator at the center of a fictive food patch. Current Biology 31, 4534-4546.e5.
doi: 10.1016/j.cub.2021.08.006.
Learning visual information to update head direction
The forensic dissection of the insect head direction system over the last years has been a beautiful success story in systems neuroscience. There is now good evidence about how the head direction system can be wired plastically to take into account environmental visual information. Here is a great looking review article giving us the current state of knowledge.
Abstract: “Animals can maintain a stable sense of direction even when they navigate in novel environments, but how the animal’s brain interprets and encodes unfamiliar sensory information in its navigation system to maintain a stable sense of direction is a mystery. Recent studies have suggested that distinct brain structures of mammals and insects have evolved to solve this common problem with strategies that share computational principles; specifically, a network structure called a ring attractor maintains the sense of direction. Initially, in a novel environment, the animal’s sense of direction relies on self-motion cues. Over time, the mapping from visual inputs to head direction cells, responsible for the sense of direction, is established via experience-dependent plasticity. Yet the mechanisms that facilitate acquiring a world-centered sense of direction, how many environments can be stored in memory, and what visual features are selected, all remain unknown. Thanks to recent advances in large scale physiological recording, genetic tools, and theory, these mechanisms may soon be revealed.”
Kim, S. S. (2021). Plasticity between visual input pathways and the head direction system. Current Opinion in Neurobiology, 71, 60-68.
Comparative Navigation
Here is a fantastic looking review, which takes a range of excellent navigators from the animal kingdom and looks for commonalities in the way that navigation is implemented at the behavioural and neural level.
Abstract: “Animals navigate a wide range of distances, from a few millimeters to globe-spanning journeys of thousands of kilometers. Despite this array of navigational challenges, similar principles underlie these behaviors across species. Here, we focus on the navigational strategies and supporting mechanisms in four well-known systems: the large-scale migratory behaviors of sea turtles and lepidopterans as well as navigation on a smaller scale by rats and solitarily foraging ants. In lepidopterans, rats, and ants we also discuss the current understanding of the neural architecture which supports navigation. The orientation and navigational behaviors of these animals are defined in terms of behavioral error-reduction strategies reliant on multiple goal-directed servomechanisms. We conclude by proposing to incorporate an additional component into this system: the observation that servomechanisms operate on oscillatory systems of cycling behavior. These oscillators and servomechanisms comprise the basis for directed orientation and navigational behaviors.”
CA Freas, K Cheng (2022) The Basis of Navigation Across Species. Annual Review of Psychology
Distributed learning
We know that the Mushroom Bodies of the insect brain are important for learning as part of foraging and navigation. However it is possible that visual learning also takes place at other places in the brain. This is strongly suggested by this study on gene expression in the insect brain.
Abstract: “Visual learning is vital to the behavioral ecology of the Western honey bee (Apis mellifera). Honey bee workers forage for floral resources, a behavior that requires the learning and long-term memory of visual landmarks, but how these memories are mapped to the brain remains poorly understood. To address this gap in our understanding, we collected bees that successfully learned visual associations in a conditioned aversion paradigm and compared gene expression correlates of memory formation in the mushroom bodies, a higher-order sensory integration center classically thought to contribute to learning, as well as the optic lobes, the primary visual neuropil responsible for sensory transduction of visual information. We quantified expression of CREB and CaMKII, two classical genetic markers of learning, and fen-1, a gene specifically associated with punishment learning in vertebrates. As expected, we found substantial involvement of the mushroom bodies for all three markers but additionally report the involvement of the optic lobes across a similar time course. Our findings imply the molecular involvement of a sensory neuropil during visual associative learning parallel to a higher-order brain region, furthering our understanding of how a tiny brain processes environmental signals.”
Avalos, A., Traniello, I. M., Claudio, E. P., & Giray, T. (2021). Parallel mechanisms of visual memory formation across distinct regions of the honey bee brain. J Exp Biol (2021) 224 (19): jeb242292.
Optic flow for flight speed independent of height
Abstract: “Honeybees foraging and recruiting nest-mates by performing the waggle dance need to be able to gauge the flight distance to the food source regardless of the wind and terrain conditions. Previous authors have hypothesized that the foragers’ visual odometer mathematically integrates the angular velocity of the ground image sweeping backward across their ventral viewfield, known as translational optic flow. The question arises as to how mathematical integration of optic flow (usually expressed in radians/s) can reliably encode distances, regardless of the height and speed of flight. The vertical self-oscillatory movements observed in honeybees trigger expansions and contractions of the optic flow vector field, yielding an additional visual cue called optic flow divergence. We have developed a self-scaled model for the visual odometer in which the translational optic flow is scaled by the visually estimated current clearance from the ground. In simulation, this model, which we have called SOFIa, was found to be reliable in a large range of flight trajectories, terrains and wind conditions. It reduced the statistical dispersion of the estimated flight distances approximately 10-fold in comparison with the mathematically integrated raw optic flow model. The SOFIa model can be directly implemented in robotic applications based on minimalistic visual equipment.”
Bergantin L, Harbaoui N, Raharijaona T, Ruffier F. 2021 Oscillations make a self-scaled model for honeybees’ visual odometer reliable regardless of flight trajectory. J. R. Soc. Interface 18: 20210567
Development, as well as sensory ecology, might shape sensors
Abstract: “Visual systems in animals often conspicuously reflect the demands of their ecological interactions. Ants occupy a wide range of terrestrial microhabitats and ecological roles. Additionally, ant eye morphology is highly variable; species range from eyeless subterranean-dwellers to highly visual predators or desert navigators. Through a comparative approach spanning 64 species, we evaluated the relationship between ecology and eye morphology on a wide taxonomic scale. Using worker caste specimens, we developed two- and three-dimensional measurements to quantify eye morphology and position, as well as antennal scape length. Surprisingly, we find limited associations between ecology and most eye traits, however, we recover significant relationships between antennal scape length and some vision-linked attributes. While accounting for shared ancestry, we find that two- and three-dimensional eye area is correlated with foraging niche and ommatidia density is significantly associated with trophic level in our sample of ant taxa. Perhaps signifying a resource investment tradeoff between visual and olfactory or tactile acuity, we find that ommatidia density is negatively correlated with antennal scape length. Additionally, we find that eye position is significantly related to antennal scape length and also report a positive correlation between scape length and eye height, which may be related to the shared developmental origin of these structures. Along with previously known relationships between two-dimensional eye size and ant ecology, our results join reports from other organismal lineages suggesting that morphological traits with intuitive links to ecology may also be shaped by developmental restrictions and energetic trade-offs.”
Jelley, C., & Barden, P. (2021). Vision-Linked Traits Associated With Antenna Size and Foraging Ecology Across Ants. Insect Systematics and Diversity, 5(5), 9.
How complex is the sensori-motor interaction in view-based navigation?
One of the most fascinating current topics in insect navigation is trying to understand the connection between sensory information and motor actions. One simple suggestion is that motor patterns act as generic drivers of sensory sampling, but many more complex interactions are possible and, indeed, likely.
Here, with an ingenious method, Woodgate et al suggest that learnt turns can be tied to a visual cue, such that information that guides a path doesn’t even need to be visible to an ant in the pathward direction.
Abstract: “The prevailing account of visually controlled routes is that an ant learns views as it follows a route, while guided by other path-setting mechanisms. Once a set of route views is memorised, the insect follows the route by turning and moving forwards when the view on the retina matches a stored view. We engineered a situation in which this account cannot suffice in order to discover whether there may be additional components to the performance of routes. One-eyed wood ants were trained to navigate a short route in the laboratory, guided by a single black, vertical bar placed in the blinded visual field. Ants thus had to turn away from the route to see the bar. They often turned to look at or beyond the bar and then turned to face in the direction of the goal. Tests in which the bar was shifted to be more peripheral or more frontal than in training produced a corresponding directional change in the ants’ paths, demonstrating that they were guided by the bar. Examination of the endpoints of turns towards and away from the bar indicate that ants use the bar for guidance by learning how large a turn-back is needed to face the goal. We suggest that the ants’ zigzag paths are, in part, controlled by turns of a learnt amplitude and that these turns are an integral component of visually guided route following.”
Woodgate, J. L., Perl, C., & Collett, T. S. (2021). The routes of one-eyed ants suggest a revised model of normal route following. Journal of Experimental Biology, 224(16), jeb242167.
Towards a fly model for path integration studies
Abstract: “The ability to keep track of one’s location in space is a critical behavior for animals navigating to and from a salient location, and its computational basis is now beginning to be unraveled. Here, we tracked flies in a ring-shaped channel as they executed bouts of search triggered by optogenetic activation of sugar receptors. Unlike experiments in open field arenas, which produce highly tortuous search trajectories, our geometrically constrained paradigm enabled us to monitor flies’ decisions to move toward or away from the fictive food. Our results suggest that flies use path integration to remember the location of a food site even after it has disappeared, and that flies can remember the location of a former food site even after walking around the arena one or more times. To determine the behavioral algorithms underlying Drosophila search, we developed multiple state transition models and found that flies likely accomplish path integration by combining odometry and compass navigation to keep track of their position relative to the fictive food. Our results indicate that whereas flies re-zero their path integrator at food when only one feeding site is present, they adjust their path integrator to a central location between sites when experiencing food at two or more locations. Together, this work provides a simple experimental paradigm and theoretical framework to advance investigations of the neural basis of path integration.”
Behbahani, A. H., Palmer, E. H., Corfas, R. A., & Dickinson, M. H. (2021). Drosophila re-zero their path integrator at the center of a fictive food patch. Current Biology. Accepted
More to learn about sensory ecology
The habitat, time of day and foraging behaviour of an insect will all contribute to the information that is available for navigation. So whilst a desert ant may scour the horizon for limited landmark information, nocturnal bees in dense forest look up to find precious information from the contrast of foliage and the night sky.
Abstract: “Bees, ants, and wasps are well known to visually navigate when traveling between their nests and foraging sites. When leaving their nest, landmarks in the vicinity are memorized and used upon return to locate the nest entrance. The Neotropical nocturnal sweat bee Megalopta genalis navigates under the forest canopy at light intensities ten times dimmer than starlight. Despite these dim conditions, Megalopta is able to memorize visual landmarks around the nest entrance in the frontal visual field. Even though frontal landmarks can clearly be discerned by Megalopta, the visual feature of greatest contrast in the rainforest at night is actually the dark dorsal silhouette of the distant canopy against the brighter night sky. Several species of ants, as well as a subsocial shield bug, use bright open gaps in the canopy as dorsal landmarks to navigate home while walking. Here we show that Megalopta is also able to distinguish dorsal landmarks during homing, the first flying insect known with this capacity. Megalopta is able to discriminate between differently oriented dorsal black striped patterns, or an “artificial canopy” of black circles, and to use this information to locate its nest entrance. These results suggest that the local foliage patterns created by the canopy against the brighter sky could potentially provide the bee with reliable landmark information for navigation during foraging and homing at night.”
Chaib, S., Dacke, M., Wcislo, W., & Warrant, E. (2021). Dorsal landmark navigation in a Neotropical nocturnal bee. Current Biology.
Insect and robot navigation 