Compass Cues Research Articles

Importance of magnetic information for neuronal plasticity in desert ants

Many animal species rely on the Earth's magnetic field during navigation, but where in the brain magnetic information is processed is still unknown. To unravel this, we manipulated the natural magnetic field at the nest entrance of Cataglyphis desert ants and investigated how this affects relevant brain regions during early compass calibration. We found that manipulating the Earth's magnetic field has profound effects on neuronal plasticity in two sensory integration centers. Magnetic field manipulations interfere with a typical look-back behavior during learning walks of naive ants. Most importantly, structural analyses in the ants' neuronal compass (central complex) and memory centers (mushroom bodies) demonstrate that magnetic information affects neuronal plasticity during early visual learning. This suggests that magnetic information does not only serve as a compass cue for navigation but also as a global reference system crucial for spatial memory formation. We propose a neural circuit for integration of magnetic information into visual guidance networks in the ant brain. Taken together, our results provide an insight into the neural substrate for magnetic navigation in insects.

A model of cue integration as vector summation in the insect brain.

Ball-rolling dung beetles are known to integrate multiple cues in order to facilitate their straight-line orientation behaviour. Recent work has suggested that orientation cues are integrated according to a vector sum, that is, compass cues are represented by vectors and summed to give a combined orientation estimate. Further, cue weight (vector magnitude) appears to be set according to cue reliability. This is consistent with the popular Bayesian view of cue integration: cues are integrated to reduce or minimize an agent's uncertainty about the external world. Integration of orientation cues is believed to occur at the input to the insect central complex. Here, we demonstrate that a model of the head direction circuit of the central complex, including plasticity in input synapses, can act as a substrate for cue integration as vector summation. Further, we show that cue influence is not necessarily driven by cue reliability. Finally, we present a dung beetle behavioural experiment which, in combination with simulation, strongly suggests that these beetles do not weight cues according to reliability. We suggest an alternative strategy whereby cues are weighted according to relative contrast, which can also explain previous results.

The use of polarized light in the zonal orientation of the sandhopper Talitrus saltator (Montagu)

It is well known that the celestial polarization is used as a compass cue by many species of insects and crustaceans. Although it has been shown that the sandhopper Talitrus saltator perceives polarized light and possesses an arrangement of the rhabdomeres that could allow e-vector interpretation and utilization, T. saltator does not use the e-vector of the skylight polarization as a compass cue when making excursions along the sea–land axis of sandy shores. We performed tests in confined conditions to clarify if skylight polarization is somehow involved in the zonal recovery of T. saltator. We observed the directional responses of sandhoppers in a transparent bowl under an artificial sky (an opaline Plexiglas dome). The bowl was covered by a blue gelatin filter with a grey filter (control condition) and a linear polarizing filter (experimental conditions) positioned under the blue one in such a way as to occupy half of the upper surface of the Plexiglas bowl so as to create a linear polarization gradient. Our experiments confirm that T. saltator perceives polarized light and highlight that this visual capability determines the perception, or perhaps the increase, of the radiance and/or spectral gradient and their use as compass cues in the zonal orientation. Moreover, our findings confirm that the radiance gradient is used as a chronometric compass orienting reference in the absence of other celestial orienting cues.

The influence of stimulus history on directional coding in the monarch butterfly brain.

The central complex is a brain region in the insect brain that houses a neural network specialized to encode directional information. Directional coding has traditionally been investigated with compass cues that revolve in full rotations and at constant angular velocities around the insect's head. However, these stimulus conditions do not fully simulate an insect's sensory perception of compass cues during navigation. In nature, an insect flight is characterized by abrupt changes in moving direction as well as constant changes in velocity. The influence of such varying cue dynamics on compass coding remains unclear. We performed long-term tetrode recordings from the brain of monarch butterflies to study how central complex neurons respond to different stimulus velocities and directions. As these butterflies derive directional information from the sun during migration, we measured the neural response to a virtual sun. The virtual sun was either presented as a spot that appeared at random angular positions or was rotated around the butterfly at different angular velocities and directions. By specifically manipulating the stimulus velocity and trajectory, we dissociated the influence of angular velocity and direction on compass coding. While the angular velocity substantially affected the tuning directedness, the stimulus trajectory influenced the shape of the angular tuning curve. Taken together, our results suggest that the central complex flexibly adjusts its directional coding to the current stimulus dynamics ensuring a precise compass even under highly demanding conditions such as during rapid flight maneuvers.

Avian navigation: the geomagnetic field provides compass cues but not a bicoordinate "map" plus a brief discussion of the alternative infrasound direction-finding hypothesis.

The geomagnetic field (GMF) is a worldwide source of compass cues used by animals and humans alike. The inclination of GMF flux lines also provides information on geomagnetic latitude. A long-disputed question, however, is whether horizontal gradients in GMF intensity, in combination with changes in inclination, provide bicoordinate "map" information. Multiple sources contribute to the total GMF, the largest of which is the core field. The ubiquitous crustal field is much less intense, but in both land and marine settings is strong enough at low altitudes (< 700m; sea level) to mask the core field's weak N-S intensity gradient (~ 3-5 nT/km) over 10s to 100s of km. Non-orthogonal geomagnetic gradients, the lack of consistent E-W gradients, and the local masking of core-field intensity gradients by the crustal field, therefore, are grounds for rejection of the bicoordinate geomagnetic "map" hypothesis. In addition, the alternative infrasound direction-finding hypothesis is briefly reviewed. The GMF's diurnal variation has long been suggested as a possible Zeitgeber (timekeeper) for circadian rhythms and could explain the GMF's non-compass role in the avian navigational system. Requirements for detection of this weaker diurnal signal (~ 20-50 nT) might explain the magnetic alignment of resting and grazing animals.

Physiological properties of the visual system in the Green Weaver ant, Oecophylla smaragdina

The Green Weaver ants, Oecophylla smaragdina are iconic animals known for their extreme cooperative behaviour where they bridge gaps by linking to each other to build living chains. They are visually oriented animals, build chains towards closer targets, use celestial compass cues for navigation and are visual predators. Here, we describe their visual sensory capacity. The major workers of O. smaragdina have more ommatidia (804) in each eye compared to minor workers (508), but the facet diameters are comparable between both castes. We measured the impulse responses of the compound eye and found their response duration (42 ms) was similar to that seen in other slow-moving ants. We determined the flicker fusion frequency of the compound eye at the brightest light intensity to be 132 Hz, which is relatively fast for a walking insect suggesting the visual system is well suited for a diurnal lifestyle. Using pattern-electroretinography we identified the compound eye has a spatial resolving power of 0.5 cycles deg−1 and reached peak contrast sensitivity of 2.9 (35% Michelson contrast threshold) at 0.05 cycles deg−1. We discuss the relationship of spatial resolution and contrast sensitivity, with number of ommatidia and size of the lens.

Intricacies of running a route without success in night-active bull ants (Myrmecia midas).

How do ants resolve conflicts between different sets of navigational cues during navigation? When two cue sets point to diametrically opposite directions, theories predict that animals should pick one set of cues or the other. Here we tested how nocturnal bull ants Myrmecia midas adjust their paths along established routes if route following does not lead to their entry into their nest. During testing, foragers were repeatedly placed back along their homeward route up to nine times, a procedure called rewinding. This procedure produced an accumulating path integrator, or vector, in diametric opposition to the learned landmark views of the route. Repeated rewinding made some individuals head initially in the nest-to-feeder vector direction, but all ants ended up using the visual scene for homing, demonstrating the importance of view-based homing in this species. Repeated rewinding, however, led to path deteriorations; with increased path meander and scanning, results also found in desert ants. After nine rewinding trips, ants were displaced off their route in further manipulations, to a site near the nest, an unfamiliar site, or with the terrestrial surround entirely covered. The results show that a change in visual conditions diminished the weight accorded to path integration: the off-route ants no longer headed off in the vector direction as they did on the immediately preceding trial. They relied on celestial compass cues in other ways for homing. Experiment 2 showed the effects of rewinding in the unaltered natural habitat were not view-specific in these bull ants. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Receptive field structures for two celestial compass cues at the input stage of the central complex in the locust brain.

Successful navigation depends on an animal's ability to perceive its spatial orientation relative to visual surroundings. Heading direction in insects is represented in the central complex (CX), a navigation center in the brain, to generate steering commands. In insects that navigate relative to sky compass signals, CX neurons are tuned to celestial cues indicating the location of the sun. The desert locust CX contains a compass-like representation of two related celestial cues: the direction of unpolarized direct sunlight and the pattern of polarized light, which depends on the sun position. Whether congruent tuning to these two compass cues emerges within the CX network or is inherited from CX input neurons is unclear. To address this question, we intracellularly recorded from GABA-immunoreactive TL neurons, which are input elements to the locust CX (corresponding to R neurons in Drosophila), while applying visual stimuli simulating unpolarized sunlight and polarized light across the hemisphere above the animal. We show that TL neurons have large receptive fields for both types of stimuli. However, faithful integration of polarization angles across the dorsal hemisphere, or matched-filter ability to encode particular sun positions, was found in only two out of 22 recordings. Those two neurons also showed a good match in sun position coding through polarized and unpolarized light signaling, whereas 20 neurons showed substantial mismatch in signaling of the two compass cues. The data, therefore, suggest that considerable refinement of azimuth coding based on sky compass signals occurs at the synapses from TL neurons to postsynaptic CX compass neurons.

Magnetosensation during re-learning walks in desert ants (Cataglyphis nodus)

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.

A Guide for Using Flight Simulators to Study the Sensory Basis of Long-Distance Migration in Insects.

Studying the routes flown by long-distance migratory insects comes with the obvious challenge that the animal’s body size and weight is comparably low. This makes it difficult to attach relatively heavy transmitters to these insects in order to monitor their migratory routes (as has been done for instance in several species of migratory birds. However, the rather delicate anatomy of insects can be advantageous for testing their capacity to orient with respect to putative compass cues during indoor experiments under controlled conditions. Almost 20 years ago, Barrie Frost and Henrik Mouritsen developed a flight simulator which enabled them to monitor the heading directions of tethered migratory Monarch butterflies, both indoors and outdoors. The design described in the original paper has been used in many follow-up studies to describe the orientation capacities of mainly diurnal lepidopteran species. Here we present a modification of this flight simulator design that enables studies of nocturnal long-distance migration in moths while allowing controlled magnetic, visual and mechanosensory stimulation. This modified flight simulator has so far been successfully used to study the sensory basis of migration in two European and one Australian migratory noctuid species.

Compass Cue Integration and Its Relation to the Visual Ecology of Three Tribes of Ball-Rolling Dung Beetles.

Simple SummaryTo escape competition for food at the dung pat, ball-rolling dung beetles shape a piece of dung into a sphere and roll it away. To maintain their bearing, these beetles integrate directional information from a range of celestial cues. For the majority of diurnal dung beetles living in open habitats, the most dominant of these cues is the sun. It has recently been demonstrated that beetles living in closed habitats, with closely spaced trees and tall grass, rely predominantly on directional information provided by polarised skylight rather than the sun. Taken together, these findings suggests that the orientation strategy of the beetle is influenced by the animal’s visual ecology. To further investigate the relative weighting of cues in the orientation system of beetles, and its relation to their visual ecology, we investigated the orientation strategy of ball-rollers from three different dung beetle tribes, all present within the same savanna biome. We find that species within a tribe share the same orientation strategy, but that this strategy differs across tribes. We conclude that, despite dramatic intertribal differences in body size and external eye design, the dynamic heading direction network of the South African ball-rolling dung beetles is well adapted to guide the foraging insect in the habitat that it normally traverses.To guide their characteristic straight-line orientation away from the dung pile, ball-rolling dung beetles steer according to directional information provided by celestial cues, which, among the most relevant are the sun and polarised skylight. Most studies regarding the use of celestial cues and their influence on the orientation system of the diurnal ball-rolling beetle have been performed on beetles of the tribe Scarabaeini living in open habitats. These beetles steer primarily according to the directional information provided by the sun. In contrast, Sisyphus fasciculatus, a species from a different dung-beetle tribe (the Sisyphini) that lives in habitats with closely spaced trees and tall grass, relies predominantly on directional information from the celestial pattern of polarised light. To investigate the influence of visual ecology on the relative weight of these cues, we studied the orientation strategy of three different tribes of dung beetles (Scarabaeini, Sisyphini and Gymnopleurini) living within the same biome, but in different habitat types. We found that species within a tribe share the same orientation strategy, but that this strategy differs across the tribes; Scarabaeini, living in open habitats, attribute the greatest relative weight to the directional information from the sun; Sisyphini, living in closed habitats, mainly relies on directional information from polarised skylight; and Gymnopleurini, also living in open habitats, appear to weight both cues equally. We conclude that, despite exhibiting different body size, eye size and morphology, dung beetles nevertheless manage to solve the challenge of straight-line orientation by weighting visual cues that are particular to the habitat in which they are found. This system is however dynamic, allowing them to operate equally well even in the absence of the cue given the greatest relative weight by the particular species.

Orcokinin in the central complex of the locust Schistocerca gregaria: Identification of immunostained neurons and colocalization with other neuroactive substances.

The central complex is a group of highly interconnected neuropils in the insect brain. It is involved in the control of spatial orientation, based on external compass cues and various internal needs. The functional and neurochemical organization of the central complex has been studied in detail in the desert locust Schistocerca gregaria. In addition to classical neurotransmitters, immunocytochemistry has provided evidence for a major contribution of neuropeptides to neural signaling within the central complex. To complement these data, we have identified all orcokinin-immunoreactive neurons in the locust central complex and associated brain areas. About 50 bilateral pairs of neurons innervating all substructures of the central complex exhibit orcokinin immunoreactivity. Among these were about 20 columnar neurons, 33 bilateral pairs of tangential neurons of the central body, and seven pairs of tangential neurons of the protocerebral bridge. In silico transcript analysis suggests the presence of eight different orcokinin-A type peptides in the desert locust. Double label experiments showed that all orcokinin-immunostained tangential neurons of the lateral accessory lobe cluster were also immunoreactive for GABA and the GABA-synthesizing enzyme glutamic acid decarboxylase. Two types of tangential neurons of the upper division of the central body were, furthermore, also labeled with an antiserum against Dip-allatostatin I. No colocalization was found with serotonin immunostaining. The data provide additional insights into the neurochemical organization of the locust central complex and suggest that orcokinin-peptides of the orcokinin-A gene act as neuroactive substances at all stages of signal processing in this brain area.

How Dung Beetles Steer Straight

Distant and predictable features in the environment make ideal compass cues to allow movement along a straight path. Ball-rolling dung beetles use a wide range of different signals in the day or night sky to steer themselves along a fixed bearing. These include the sun, the Milky Way, and the polarization pattern generated by the moon. Almost two decades of research into these remarkable creatures have shown that the dung beetle's compass is flexible and readily adapts to the cues available in its current surroundings. In the morning and afternoon, dung beetles use the sun to orient, but at midday, they prefer to use the wind, and at night or in a forest, they rely primarily on polarized skylight to maintain straight paths. We are just starting to understand the neuronal substrate underlying the dung beetle's compass and the mystery of why these beetles start each journey with a dance.

The effect of step size on straight-line orientation.

Moving along a straight path is a surprisingly difficult task. This is because, with each ensuing step, noise is generated in the motor and sensory systems, causing the animal to deviate from its intended route. When relying solely on internal sensory information to correct for this noise, the directional error generated with each stride accumulates, ultimately leading to a curved path. In contrast, external compass cues effectively allow the animal to correct for errors in its bearing. Here, we studied straight-line orientation in two different sized dung beetles. This allowed us to characterize and model the size of the directional error generated with each step, in the absence of external visual compass cues (motor error) as well as in the presence of these cues (compass and motor errors). In addition, we model how dung beetles balance the influence of internal and external orientation cues as they orient along straight paths under the open sky. We conclude that the directional error that unavoidably accumulates as the beetle travels is inversely proportional to the step size of the insect, and that both beetle species weigh the two sources of directional information in a similar fashion.

Multimodal cue integration in the dung beetle compass

South African ball-rolling dung beetles exhibit a unique orientation behavior to avoid competition for food: after forming a piece of dung into a ball, they efficiently escape with it from the dung pile along a straight-line path. To keep track of their heading, these animals use celestial cues, such as the sun, as an orientation reference. Here we show that wind can also be used as a guiding cue for the ball-rolling beetles. We demonstrate that this mechanosensory compass cue is only used when skylight cues are difficult to read, i.e., when the sun is close to the zenith. This raises the question of how the beetles combine multimodal orientation input to obtain a robust heading estimate. To study this, we performed behavioral experiments in a tightly controlled indoor arena. This revealed that the beetles register directional information provided by the sun and the wind and can use them in a weighted manner. Moreover, the directional information can be transferred between these 2 sensory modalities, suggesting that they are combined in the spatial memory network in the beetle's brain. This flexible use of compass cue preferences relative to the prevailing visual and mechanosensory scenery provides a simple, yet effective, mechanism for enabling precise compass orientation at any time of the day.

Straight-line orientation in the woodland-living beetle Sisyphus fasciculatus

To transport their balls of dung along a constant bearing, diurnal savannah-living dung beetles rely primarily on the sun for compass information. However, in more cluttered environments, such as woodlands, this solitary compass cue is frequently hidden from view by surrounding vegetation. In these types of habitats, insects can, instead, rely on surrounding landmarks, the canopy pattern, or wide-field celestial cues, such as polarised skylight, for directional information. Here, we investigate the compass orientation strategy behind straight-line orientation in the diurnal woodland-living beetle Sisyphus fasciculatus. We found that, when manipulating the direction of polarised skylight, Si. fasciculatus responded to this change with a similar change in bearing. However, when the apparent position of the sun was moved, the woodland-living beetle did not change its direction of travel. In contrast, the savannah-living beetle Scarabaeus lamarcki responded to the manipulation of the solar position with a corresponding change in bearing. These results suggest that the dominant compass cue used for straight-line orientation in dung beetles may be determined by the celestial cue that is most prominent in their preferred habitat.

Two Compasses in the Central Complex of the Locust Brain.

Many migratory insects rely on a celestial compass for spatial orientation. Several features of the daytime sky, all generated by the sun, can be exploited for navigation. Two of these are the position of the sun and the pattern of polarized skylight. Neurons of the central complex (CX), a group of neuropils in the central brain of insects, have been shown to encode sky compass cues. In desert locusts, the CX holds a topographic, compass-like representation of the plane of polarized light (E-vector) presented from dorsal direction. In addition, these neurons also encode the azimuth of an unpolarized light spot, likely representing the sun. Here, we investigate whether, in addition to E-vector orientation, the solar azimuth is represented topographically in the CX. We recorded intracellularly from eight types of CX neuron while stimulating animals of either sex with polarized blue light from zenithal direction and an unpolarized green light spot rotating around the animal's head at different elevations. CX neurons did not code for elevation of the unpolarized light spot. However, two types of columnar neuron showed a linear correlation between innervated slice in the CX and azimuth tuning to the unpolarized green light spot, consistent with an internal compass representation of solar azimuth. Columnar outputs of the CX also showed a topographic representation of zenithal E-vector orientation, but the two compasses were not linked to each other. Combined stimulation with unpolarized green and polarized blue light suggested that the two compasses interact in a nonlinear way.SIGNIFICANCE STATEMENT In the brain of the desert locust, neurons sensitive to the plane of celestial polarization are arranged like a compass in the slices of the central complex (CX). These neurons, in addition, code for the horizontal direction of an unpolarized light cue possibly representing the sun. We show here that horizontal directions are, in addition to E-vector orientations from the dorsal direction, represented in a compass-like manner across the slices of the CX. However, the two compasses are not linked to each other, but rather seem to interact in a cell-specific, nonlinear way. Our study confirms the role of the CX in signaling heading directions and shows that different cues are used for this task.

The brain behind straight-line orientation in dung beetles.

For many insects, celestial compass cues play an important role in keeping track of their directional headings. One well-investigated group of celestial orientating insects are the African ball-rolling dung beetles. After finding a dung pile, these insects detach a piece, form it into a ball and roll it away along a straight path while facing backwards. A brain region, termed the central complex, acts as an internal compass that constantly updates the ball-rolling dung beetle about its heading. In this review, we give insights into the compass network behind straight-line orientation in dung beetles and place it in the context of the orientation mechanisms and neural networks of other insects. We find that the neuronal network behind straight-line orientation in dung beetles has strong similarities to the ones described in path-integrating and migrating insects, with the central complex being the key control point for this behavior. We conclude that, despite substantial differences in behavior and navigational challenges, dung beetles encode compass information in a similar way to other insects.

Neuroarchitecture of the dung beetle central complex.

Despite their tiny brains, insects show impressive abilities when navigating over short distances during path integration or during migration over thousands of kilometers across entire continents. Celestial compass cues often play an important role as references during navigation. In contrast to many other insects, South African dung beetles rely exclusively on celestial cues for visual reference during orientation. After finding a dung pile, these animals cut off a piece of dung from the pat, shape it into a ball and roll it away along a straight path until a suitable place for underground consumption is found. To maintain a constant bearing, a brain region in the beetle's brain, called the central complex, is crucially involved in the processing of skylight cues, similar to what has already been shown for path-integrating and migrating insects. In this study, we characterized the neuroanatomy of the sky-compass network and the central complex in the dung beetle brain in detail. Using tracer injections, combined with imaging and 3D modeling, we describe the anatomy of the possible sky-compass network in the central brain. We used a quantitative approach to study the central-complex network and found that several types of neuron exhibit a highly organized connectivity pattern. The architecture of the sky-compass network and central complex is similar to that described in insects that perform path integration or are migratory. This suggests that, despite their different orientation behaviors, this neural circuitry for compass orientation is highly conserved among the insects.

The Dung Beetle Compass

What do a burly rower, a backstroke swimmer and a hard-working South African dung beetle all have in common? The answer is: they all benefit from moving along a straight path, and do so moving backwards. This, however, is where the similarity ends. While the rower has solved this navigational challenge by handing the task of steering to the coxswain, who faces the direction of travel, and the swimmer is guided down her lane by colourful ropes, the beetle puts its faith in the sky. From here, it utilises a larger repertoire of celestial compass cues than is known to be used by any other animal studied to date. A robust internal compass, designed to interpret directional information, has evolved under the selective pressure of shifting today's lunch efficiently out of reach of competitors, also drawn to the common buffet. While this is a goal that beetles might share with the hungry athletes, they reach it with drastically different brain powers; the brain of the beetle is several times smaller than a match head, containing fewer than a million neurons.