Seeing and not seeing

Recent studies revealed that although subterranean mammals inhabit a dark underground environment, they can still perceive light stimuli and use this to entrain their circadian activity rhythm. Regarding spatial orientation, olfactory and tactile cues are employed for short-distance; whereas for long-distance, subterranean mammals employ the earth's magnetic field and self-generated (vestibular and kinestatic) cues. We suggest that seismic signals, utilized for long-distance communication, might also be used as an echolocation mechanism to determine digging depth and presence of obstacles ahead. Taken together, these mechanisms provide an equally efficient means of overall orientation and communication as those found in sighted mammals.     

Experimental evidence for geomagnetic orientation in juvenile salmon, Oncorhynchus tschawytscha Walbaum

Juvenile chinook salmon, Oncorhynchus tschawytscha , kept under artificial light in a rectangular holding tank aligned east/west for 18 months, showed a preferred temporal and directional orientation of 270° with respect to water flow and the source of food.
Individual fish transferred from the holding/training tank to an unfamiliar circular test arena in another room devoid of local directional cues showed a mean of means preferred unimodal orientation of 264°.
Controlled re-introduction of individual stimuli revealed a hierarchy of orientation cues; one of these was a response to magnetism. A 90° clockwise shift in the horizontal component of the earth's magnetic field was followed by a significant change in the mean of means axial orientation, for the fish under test, from 258°/78° to 354°/174°. After restoration of the normal magnetic field the mean of means axial orientation reverted to 274°/94°.     

Magnetic Orientation in the Savannah Sparrow

Although magnetic compass orientation has been reported in a number of invertebrate and vertebrate taxa, including about a dozen migratory bird species, magnetic orientation capabilities in animals remain somewhat controversial. We have hand-raised a large number of Savannah sparrows (Passerculus sandwichensis) to study the ontogeny of orientation behavior. Young birds with a variety of early experience with visual and magnetic orientation cues have been tested for magnetic orientation during their first autumn migration. Here we present data from 80 hand-raised sparrows, each tested several times in both normal and shifted magnetic fields. Birds reared indoors with no experience with visual orientation cues showed axial north-south orientation that shifted by almost exactly the magnitude of 90° clockwise and counterclockwise shifts in the direction of magnetic north. Other groups of birds with varying early experience with visual orientation cues showed different preferred orientation directions, but all groups shifted orientation direction in response to shifts in the magnetic field. The data thus demonstrate a robust magnetic orientation ability in this species.     

Attentional bias to food images associated with elevated weight and future weight gain: an fMRI study

Behavioral studies reveal that obese vs. lean individuals show attentional bias to food stimuli. Yet research has not investigated this relation using objective brain imaging or tested whether attentional bias to food stimuli predicts future weight gain, which are important aims given the prominence of food cues in the environment. We used functional magnetic resonance imaging (fMRI) to examine attentional bias in 35 adolescent girls ranging from lean to obese using an attention network task involving food and neutral stimuli. BMI correlated positively with speed of behavioral response to both appetizing food stimuli and unappetizing food stimuli, but not to neutral stimuli. BMI correlated positively with activation in brain regions related to attention and food reward, including the anterior insula/frontal operculum, lateral orbitofrontal cortex (OFC), ventrolateral prefrontal cortex (vlPFC), and superior parietal lobe, during initial orientation to food cues. BMI also correlated with greater activation in the anterior insula/frontal operculum during reallocation of attention to appetizing food images and with weaker activation in the medial OFC and ventral pallidum during reallocation of attention to unappetizing food images. Greater lateral OFC activation during initial orientation to appetizing food cues predicted future increases in BMI. Results indicate that overweight is related to greater attentional bias to food cues and that youth who show elevated reward circuitry responsivity during food cue exposure are at increased risk for weight gain.     

Orientation by magnetic field in leaf-cutter ants, Atta colombica (Hymenoptera: Formicidae)

Leaf‐cutter ants (Atta colombica) use trail following to travel between foraging sites and the home nest. However, this combination of pheromone and visual cues is likely to be complemented by a directional reference system such as a compass, used not only when foraging but also during colony formation, where foraging trails degrade or where ants become displaced. One candidate system is the magnetic polarity compass. We tested the orientation of leaf‐cutter ants under a magnetic field of reversed‐polarity, with the prediction that the ants would show 180° deflection compared with control ants in an unchanged geomagnetic field. When the sun's disc was unobstructed by clouds, orientation was the same as that of control ants, implying that magnetic cues were not used to orient. However, when the sky was overcast, ants in the experimental treatment significantly shifted their mean orientation both in comparison with controls and reversed‐polarity ants under the sun. Although a total reversal in orientation was not induced, the results demonstrate that Atta respond to magnetic reversal in the absence of sunlight cues, and suggest a role for magnetic cues in determining direction during orientation.     

A comprehensive hypothesis on the migration of European glass eels (Anguilla anguilla)

The European eel (Anguilla anguilla) is a catadromous fish that spawns in the Sargasso Sea. As larvae, eels cross the Atlantic Ocean and reach the continental slope of Europe, where they metamorphose into post‐larval glass eels. These reach the continent, where some enter fresh water, some remain in marine waters, and others move between fresh and marine waters. After 5–25 years, as adult silver eels, they migrate back from fresh water to the Sargasso Sea to spawn and die. The glass eel stage is a critical step during which the eels cross the continental shelf and recruit to estuaries, where they facultatively transition to fresh water. Extensive research has been conducted to understand the behavioural mechanisms and environmental cues that aid and guide glass eels' migration. Glass eels follow odours and salinity gradients, they avoid light, and they change orientation and depth according to the tides. Recent work revealed that European glass eels also use Earth's magnetic field and lunar cues to orient. However, while we understand many aspects of their orientation behaviour, a unifying theory describing how glass eels migrate from the continental slope to fresh water is lacking. The goal of this review is to develop a comprehensive hypothesis on the migration of European glass eels, integrating previous knowledge on their orientation behaviour with recent findings on magnetic and celestial orientation. This review follows the journey of a hypothetical glass eel, describing the nature and the role of orientation cues involved at each step. I propose that, although glass eels have the sensory capacity to use multiple cues at any given time, their migration is based on a hierarchical succession of orientation mechanisms dictated by the physical properties of the environments that they occupy: (i) lunar and magnetic cues in pelagic water; (ii) chemical and magnetic cues in coastal areas; and (iii) odours, salinity, water current and magnetic cues in estuaries.     

Magnetic maps in animals: a theory comes of age?

The magnetic map hypothesis proposes that animals can use spatial gradients in the Earth's magnetic field to help determine geographic location. This ability would permit true navigation--reaching a goal from an entirely unfamiliar site with no goal-emanating cues to assist. It is a highly contentious hypothesis since the geomagnetic field fluctuates in time and spatial gradients may be disturbed by geological anomalies. Nevertheless, a substantial body of evidence offers support for the hypothesis. Much of the evidence has been indirect in nature, such as the identification of avian magnetoreceptor mechanisms with functional properties that are consistent with those of a putative map detector or the patterns of orientation of animals exposed to temporal and/or spatial geomagnetic anomalies. However; the most important advances have been made in conducting direct tests of the magnetic map hypothesis by exposing experienced migrants to specific geomagnetic values representing simulated displacements. Appropriate shifts in the direction of orientation, which compensate for the simulated displacements, have been observed in newts, birds, sea turtles, and lobsters, and provide the strongest evidence to date for magnetic map navigation. Careful experimental design and interpretation of orientation data will be essential in the future to determine which components of the magnetic field are used to derive geographic position.     

Compass orientation and possible migration routes of passerine birds at high arctic latitudes

The use of celestial or geomagnetic orientation cues can lead migratory birds along different migration routes during the migratory journeys, e.g. great circle routes (approximate), geographic or magnetic loxodromes. Orientation cage experiments have indicated that migrating birds are capable of detecting magnetic compass information at high northern latitudes even at very steep angles of inclination. However, starting a migratory journey at high latitudes and following a constant magnetic course often leads towards the North Magnetic Pole, which means that the usefulness of magnetic compass orientation at high latitudes may be questioned. Here, we compare possible long‐distance migration routes of three species of passerine migrants breeding at high northern latitudes. The initial directions were based on orientation cage experiments performed under clear skies and simulated overcast and from release experiments under natural overcast skies. For each species we simulated possible migration routes (geographic loxodrome, magnetic loxodrome and sun compass route) by extrapolating from the initial directions and assessing a fixed orientation according to different compass mechanisms in order to investigate what orientation cues the birds most likely use when migrating southward in autumn. Our calculations show that none of the compass mechanisms (assuming fixed orientation) can explain the migration routes followed by night‐migrating birds from their high Nearctic breeding areas to the wintering sites further south. This demonstrates that orientation along the migratory routes of arctic birds (and possibly other birds as well) must be a complex process, involving different orientation mechanisms as well as changing compass courses. We propose that birds use a combination of several compass mechanisms during a migratory journey with each of them being of a greater or smaller importance in different parts of the journey, depending on environmental conditions. We discuss reasons why birds developed the capability to use magnetic compass information at high northern latitudes even though following these magnetic courses for any longer distance will lead them along totally wrong routes. Frequent changes and recalibrations of the magnetic compass direction during the migratory journey are suggested as a possible solution.     

Development and organization of multimodal representation in cat superior colliculus

The present paper examines developmental and organizational parallels between visual and nonvisual cells in the cat superior colliculus (SC). An attempt is made to relate these developmental and organizational features to the role the SC plays in orientation behavior. In young kittens visually guided behavior is virtually nonexistent and requires many weeks to develop. Similarly, kitten SC cells are unresponsive to visual stimuli until at least 7 days after birth, and it is only after many weeks that SC cells behave as do those of the adult. In contrast to the development of visual cells, however, some neurons responsive to somatic stimuli are present in the SC on the day of birth, and cells responsive to acoustic stimuli appear several days later. Thus, the sequence in which modality represenstation appears in the cat SC parallels the developmental chronology of the use of different sensory cues for orientation. These data indicate that the functional roles of the visual, somatic, and acoustic representations may be similar. The finding that the organization of the somatic representation in the SC is similar to, and in register with, the visual representation is consistent with this possibility. It is suggested that the SC can utilize cues from a variety of modalities in order to facilitate appropriate orientation behavior.     

Integration of environmental stimuli in the migratory orientation of the savannah sparrow (Passerculus sandwichensis)

Two ‘cue-conflict’ experiments were designed to evaluate the role of (1) solar cues at sunset and stars, and (2) solar cues at sunset and geomagnetic stimuli, in the migratory orientation of the savannah sparrow (Passerculus sandwichensis). A sunset and stars experiment exposed birds in the experimental group to a mirror-reflected sunset followed by an unmanipulated view of stars. Experimental birds shifted their migratory activity in accordance with the setting sun despite exposure to a normal night sky. The sunset and geomagnetism experiment exposed birds in the experimental group to a simultaneous shift in both the position of sunset and the earth's magnetic field. Again experimentals shifted their activity in accordance with the setting sun rather than the artificially shifted magnetic field. Savannah sparrows probaly use stars as celestial landmarks to maintain a preferred direction and do not reorient their activity when exposed to an alternative cue once a direction is established. Moreover, savannah sparrows with experience of migration do not require geomagnetic information in order to use the solar cues available at sunset to select a migratory direction.     

SUNSET AND THE ORIENTATION BEHAVIOUR OF MIGRATING BIRDS

1. Migratory birds integrate information from a wide array of environmental sources. As our knowledge of migratory orientation depends heavily upon the results of cage-experiments with nocturnal migrants, it is essential that the results of these cage studies be interpreted in the light of field observations of migratory behaviour and experiments with free-flying migrants. When this is done, the impression emerges that night-migrating birds integrate directional information prior to departure, probably during the transition between daylight and darkness. At this time, information gained from the sun, in conjunction with other references, becomes especially valuable. 2. Despite intensive work with a few species, how migrants integrate information in the selection and maintenance of a direction is not well understood. The relationship between magnetic stimuli and solar cues at sunset in the selection process, for example, remains to be resolved, as does the contribution of skylight polarization patterns at sunset. Once a migratory heading is selected, birds probably use the stars or winds aloft to maintain that direction. How migrants integrate information is largely a matter of unravelling the complex causal relations among the different environmental stimuli that serve as orientation cues. Imagine a hypothetical migrant that departs on a migratory flight around the time of sunset. Given the uncertain relationship among variables (orientation cues) that might influence her migratory orientation, a path diagram is a useful device for displaying graphically the pattern of causal relations among the set of variables (see Fig. 1). This technique is adopted from path analysis, which is a statistical method developed by Sewall Wright for studying the direct and indirect causal relations among variables (see Kerlinger & Pedhazur, 1973). The pattern depicted in the figure is less a specific model of causal relations than it is a summary of possible relationships among the several cues based on current understanding. Causal flow in this ‘model’ is unidirectional, i.e. at any given point in time a variable cannot be both a cause and an effect of another variable. For example, variable 3 is dependent on variables 1 and/or 2, and is one of the independent variables in relation to variable 5 (orientation of migratory activity). Although the value of path analysis to the study of migratory orientation may be largely heuristic at this point, ‘one virtue of the method is that in order to apply it the researcher is required to make explicit the theoretical framework within which he operates’ (Kerlinger & Pedhazur, 1973). For instance, path diagrams (and path analysis, to the degree that correlations between variables can be specified) would help researchers study (i) the apparent redundancy built into the orientation process (see Fig. 1), (ii) alternative or competing causal models of orientation and navigation, or (iii) the ontogenetic changes that affect the relationship among orientation variables. Imagine, for example, how path coefficients might change in value with migratory experience. 3. Migrants probably redetermine preferred directions soon after landing or shortly before their next departure rather than while aloft. Cage-orientation results as well as observations of free-flying migrants suggest that solar-related information is involved in the morning orientation of ongoing migratory flight and possibly the re-determination of direction following night-time displacement. 4. Evidence is not clear on whether migrants respond to sunset by constant-angle orientation (menotaxis) or constant-azimuth orientation. 5. How migrants correctly identify sunset as a reference stimulus is an unresolved question. Identification might be based upon the characteristic spectral distribution of sunset, its pattern of illumination, or some other feature, such as the characteristic pattern of skylight polarization at sunset. 6. Several lines of evidence suggest that migrants learn to use the setting sun and associated skylight features as orientation cues. 7. The setting sun functions not only as a source of directional information but also as an environmental stimulus that influences the likelihood of migratory activity.     

Magnetic Orientation in Solenopsis sp. Ants

It is known that magnetic fields affect ants behavior. It has been shown that Solenopsis ants are sensitive to magnetic fields but there is no experimental evidence for magnetic orientation. In this paper experiments were done to verify the magnetic orientation of Solenopsis sp. ants. The spontaneous orientation of ants in a circular arena was studied in two different magnetic conditions: in the natural geomagnetic field and under an altered magnetic field, with the horizontal geomagnetic axis shifted in 90?o. Our results show that ants consistently change their orientation direction when the magnetic field was altered. Axial circular statistics analysis showed that, in the absence of other cues, ants orient spontaneously to the horizontal geomagnetic field axis. The present paper shows for the first time magnetic orientation in Solenopsis sp. ants.     

Innate preference for magnetic compass direction in the Alpine newt, <Emphasis Type="Italic">Triturus alpestris</Emphasis> (Salamandridae,Urodela)?

Magnetic compass orientation was first discovered for migrating/homing birds in which all individuals of a population or species prefer a predictable magnetic direction during a particular migratory situation. If all other sensory cues are absent, the Earth’s magnetic field may serve as a reference for other orientation mechanisms. It will be demonstrated that alpine newts (Triturus alpestris, Salamandridae) spontaneously align according to the natural or the deviated magnetic field lines of the Earth. They are able to do this in the dark and by apparently seeking to maintain a specific angle with respect to the magnetic field vector. When the horizontal component of the magnetic vector was eliminated, animals became disoriented, and orientation became random. We infer that the animals observed had learned to prefer a particular magnetic direction following environmental/geographical cues. Alternatively, the magnetic directional alignments are innate as, e.g. in migrating birds, but these may be modified/altered according to season, age, hormonal status, and environmental factors such as “landmarks”, light-, sound-, or olfactory cues. Numerous observations of the aligning showed that the preference for a certain magnetic compass direction/axis was not only individual but also specific for the population-subgroups tested. Specimens roughly preferred magnetic directions close to east or west. However, the larvae were able to learn to align to obviously attractive hiding spots (tubes) that were provided in a direction that deviated with respect to the first magnetic preference. The new conditioned alignments were, again, referred to magnetically by the animals and remained stable, even if the hiding tubes were absent. Animals preferred that direction until, eventually, a new directional cue became attractive.     

Magnetic Compass Orientation in Larval Iberian Green Frogs, Pelophylax Perezi

Experiments were carried out to investigate whether Iberian green frog tadpoles Pelophylax perezi (formerly Rana perezi) are able of using the geomagnetic field for y‐axis orientation (i.e. orientation toward and away from shore). Tadpoles were trained outdoor for 5 d, in two different training configurations: (i) a training tank aligned along the magnetic north–south axis, with shore facing south, and (ii) a training tank aligned along the magnetic east–west axis, with shore located east, and similar to the shore–deep water axis (‘y‐axis’) found in their home stream, which flows from south to north. After training, tadpoles were individually tested for magnetic orientation in a water‐filled circular outdoor arena surrounded by a pair of orthogonally aligned cube‐surface‐coils used to alter the alignment of the earth's magnetic field. Tadpoles held in the east–west training tank oriented towards shore, indicating that they were able to distinguish between the shoreward and waterward direction along the y‐axis. Tadpoles trained in the tank that was aligned along the north–south axis showed bimodal magnetic compass orientation along the shore–deep water magnetic axis. These findings provide evidence for the use of magnetic compass cues for y‐axis orientation by P. perezi tadpoles.     

Rapid Learning of Magnetic Compass Direction by C57BL/6 Mice in a 4-Armed ‘Plus’ Water Maze

Magnetoreception has been demonstrated in all five vertebrate classes. In rodents, nest building experiments have shown the use of magnetic cues by two families of molerats, Siberian hamsters and C57BL/6 mice. However, assays widely used to study rodent spatial cognition (e.g. water maze, radial arm maze) have failed to provide evidence for the use of magnetic cues. Here we show that C57BL/6 mice can learn the magnetic direction of a submerged platform in a 4-armed (plus) water maze. Naïve mice were given two brief training trials. In each trial, a mouse was confined to one arm of the maze with the submerged platform at the outer end in a predetermined alignment relative to magnetic north. Between trials, the training arm and magnetic field were rotated by 180^° so that the mouse had to swim in the same magnetic direction to reach the submerged platform. The directional preference of each mouse was tested once in one of four magnetic field alignments by releasing it at the center of the maze with access to all four arms. Equal numbers of responses were obtained from mice tested in the four symmetrical magnetic field alignments. Findings show that two training trials are sufficient for mice to learn the magnetic direction of the submerged platform in a plus water maze. The success of these experiments may be explained by: (1) absence of alternative directional cues (2), rotation of magnetic field alignment, and (3) electromagnetic shielding to minimize radio frequency interference that has been shown to interfere with magnetic compass orientation of birds. These findings confirm that mice have a well-developed magnetic compass, and give further impetus to the question of whether epigeic rodents (e.g., mice and rats) have a photoreceptor-based magnetic compass similar to that found in amphibians and migratory birds.     

Contextual taste cues modulate olfactory learning in C. elegans by an occasion-setting mechanism

Manipulations of context can affect learning and memory performance across species in many associative learning paradigms. Using taste cues to create distinct contexts for olfactory adaptation assays in the nematode Caenorhabditis elegans, we now show that performance in this associative learning paradigm is sensitive to context manipulations, and we investigate the mechanism(s) used for the integration of context cues in learning. One possibility is that the taste and olfactory stimuli are perceived as a combined, blended cue that the animals then associate with the unconditioned stimulus (US) in the same manner as with any other unitary conditioned stimuli (CS). Alternatively, an occasion-setting model suggests that the taste cues only define the appropriate context for olfactory memory retrieval without directly entering into the primary association. Analysis of genetic mutants demonstrated that the olfactory and context cues are sensed by distinct primary sensory neurons and that the animals' ability to use taste cues to modulate olfactory learning is independent from their ability to utilize these same taste cues for adaptation. We interpret these results as evidence for the occasion-setting mechanism in which context cues modulate primary Pavlovian association by functioning in a hierarchical manner to define the appropriate setting for memory recall.     

Geomagnetic information modulates nocturnal migratory restlessness but not fueling in a long distance migratory songbird

Geomagnetic cues have been shown to influence migratory orientation and migratory fuelling in night‐migratory songbird species. Here, we used captive‐bred northern wheatears Oenanthe oenanthe from the southern Norwegian population to show that other aspects of the birds’ migratory program can be influenced by magnetic cues as well. We observed that the amount of migratory restlessness increased strongly with progression of the migratory season when the birds were kept constantly in the magnetic field of northern Germany, but the amount of migratory restlessness decreased when the magnetic field changed along the birds’ natural flyway are simulated. Thus, the Earth's magnetic field can also act as a ‘signpost’ cue for fine‐tuning the spatio‐temporal course of migration.     

Tolerance to morphine-induced analgesia in mice: Magnetic fields function as environmental specific cues and reduce tolerance development

Mice receiving daily injection of morphine (10 mg/kg) developed tolerance to morphine-induced analgesia, such that after 5–7 days of treatment their thermal response (paw licking) latencies in the hot plate test were indistinguishable from those of control animals. Exposure to a rotating magnetic field for thirty minutes before the daily morphine administrations significantly reduced the development of tolerance. These magnetic exposure also significantly increased over 7–10 days the basal nociceptive thresholds and paw licking response latencies of saline treated mice. Control and sham exposed mice that were fully tolerant to the analgesic effects of morphine failed to show any tolerance to morphine-induced analgesia when exposed to the magnetic stimuli prior to injection. Likewise, the partial tolerance to morphine shown by mice exposed to the rotating magnetic field pre-injection environmental cues was eliminated when control or sham pre-injection cues lacking the magnetic stimuli were provided. In all cases tolerance to morphine-induced analgesia was evident in the subsequent re-test with the original cues. These results indicate that magnetic field exposure can reduce the development of tolerance to the analgesic effects of morphine. They also show that magnetic stimuli function as significant environmental cues for the development of tolerance to morphine-induced analgesia. This suggests that magnetic stimuli affect both the associative (classical conditioning) and non-associative (physiological, pharmacological) mechanisms involved in the development of opiate tolerance.     

Role of chemical and visual cues in food recognition by leatherback posthatchlings (Dermochelys coriacea L)

We raised leatherback posthatchlings in the laboratory for up to 7 weeks to study the role of visual and chemical cues in food recognition and food-seeking behavior. Turtles were reared on a formulated (artificial gelatinous) diet and had no contact with test materials until experiments began. Subjects were presented with visual cues (a plastic jellyfish; white plastic shapes [circle, square, diamond] similar in surface area to the plastic model), chemical cues (homogenates of lion's mane jellyfish, Cyanea capillata; moon jellyfish, Aurelia aurita; and a ctenophore, Ocyropsis sp., introduced through a water filter outflow), and visual and chemical cues presented simultaneously. Visual stimuli evoked an increase in swimming activity, biting, diving, and orientation toward the object. Chemical cues elicited an increase in biting, and orientation into water currents (rheotaxis). When chemical and visual stimuli were combined, turtles ignored currents and oriented toward the visual stimuli. We conclude that both cues are used to search for, and locate, food but that visual cues may be of primary importance. We hypothesize that under natural conditions turtles locate food visually, then, as a consequence of feeding, associate chemical with visual cues. Chemical cues then may function alone as a feeding attractant.     

Pineal Body and Magnetic Sensitivity: Homing in Pinealectomized Pigeons under Overcast Skies

Since birds use the earth's magnetic field for compass orientation when astronomical cues are lacking and it has recently been suggested that the pineal body is part of their magnetic compass, test releases have been performed in overcast conditions with pigeons deprived of the pineal body. On the whole, both experimental and control birds were capable of homeward orientation, though the bearings of experimental were rather more scattered. No differences in homing speed or success were recorded. Thus, the pineal body does not appear to play an important role in the homing of pigeons.