The neural mechanisms of long distance animal navigation

Barrie J Frost1 and Henrik Mouritsen2
Animal navigation is a complex process involving the integration of many sources of specialized sensory information for navigation in near and far space. Our understanding of the neurobiological underpinnings of near-space navigation is welldeveloped, whereas the neural mechanisms of long-distance navigation are just beginning to be unraveled. One crucial question for future research is whether the near space concepts of place cells, head direction cells, and maps in the entorhinal cortex scale up to animals navigating over very long distances and whether they are related to the map and compass concepts of long-distance navigation.
Addresses 1 Department of Psychology, Queen’s University, Kingston, Ontario, K7L 3N6, Canada 2 VW-Nachwuchsgruppe Animal Navigation, Institute of Biology and Environmental Sciences, University of Oldenburg, D-26111 Oldenburg, Germany Corresponding author: Frost, Barrie J (

and reliability of the different cues. Animals are often able to sense and use more cues than they ‘need’ for a given navigational task, and they might or might not use a given cue in a given experimental setup or situation. This complicates the study of animal navigation and can lead to seemingly contradictory findings. Historically, there appears to be a great divide between scientists studying ‘near space’ and ‘far space’ navigation mechanisms, in terms of the model species they study, the methods they employ, and the theoretical models they derive [6]. However, because any long-distance navigation task, for instance a migratory journey, includes both homing and goal pin-pointing phases (e.g. [2,7]), the mechanisms used for near-space navigation are also relevant for migration. There are many excellent reviews covering the problem of near space navigation of many species (e.g. [8,9,10–14]). In this brief review, we focus primarily on recent progress related to the rather elusive mechanisms underlying navigation over large distances, and discuss whether some of the well-studied neural mechanisms of near-space navigation might also be used in the long-distance navigation phase of migration.

Current Opinion in Neurobiology 2006, 16:481–488 This review comes from a themed issue on Sensory systems Edited by Yang Dan and Richard D Mooney Available online 12th July 2006 0959-4388/$ – see front matter # 2006 Elsevier Ltd. All rights reserved. DOI 10.1016/j.conb.2006.06.005

The navigational problem
Most navigational tasks require that an animal first determines its current spatial location relative to some distant goal such as its nest, territory, food cache, or wintering ground (typically referred to as ‘map’ information). Once position has been determined, an animal chooses the appropriate direction of travel (‘compass’ stage) to most efficiently reach that goal [6].

Navigation is one of the most complex facets of animal behavior. It includes both navigation within the local space provided by their ‘home range’ habitat and the ability of some species to relocate to distant seasonal target areas. Three striking examples of long distance navigation are the 11,000 Km non-stop migration of bartailed godwits [1] from Alaska across the Pacific Ocean to New Zealand, the reoccurrence of individual migrants on the same stop-over localities year after year [2,3] and the 3,400 Km fall migration of Monarch butterflies from Canada to Central Mexico [4,5]. ‘Homing’ and ‘migratory’ behaviors clearly occur in both invertebrate and vertebrate species alike, and although some of the problems to be solved are generic, others are very specific adaptations to particular niches and lifestyles, which means that the mechanisms used to solve the navigation tasks could differ dramatically among species. Furthermore, multiple sources of navigational information must be integrated and the weighting of these sources will probably change dynamically with the demands of the task and availability

In familiar space, map information can be based on a large variety of previously encountered cues. These cues could include visual landmarks, olfactory cues, local magnetic variations and auditory information, and which specific cues are used can vary dramatically among species, tasks, and even among individuals. In near- to medium-distance unfamiliar space (navigation within this space is normally termed ‘homing’), the extrapolation of familiar cues that form reasonably consistent gradients within the familiar space is likely to play a major role in navigation. Which cues provide the most reliable gradients in a given area will vary regionally, and thus the cues that the animals prefer are also expected to vary. Recent studies have shown how, for example, gradients of odors (e.g. [15,16,17]), magnetic intensity and/or inclination [18,19–22] can provide animals with some basic form of map information. Another navigational mechanism that
Current Opinion in Neurobiology 2006, 16:481–488

38].com . such as the geomagnetic field.27]. young birds on their first autumn migration use a ‘vector navigation’ or ‘calendar-and-compass’ strategy. Obviously landmark and PI information need to be integrated into map-like representations [12]. motor and proprioceptive systems are considered the primary sources of this selfmotion information. 16:481–488 Celestial information The sun Many experiments continue to show that some form of time-compensated sun-compass plays a crucial role in www. Our understanding of the neurobiology of maps has been advanced yet again by the recent findings of Hafting et al.and far space divide to investigate this possibility. and because path integration is prone to increasing errors with distance. Moreover. Different cells exhibit either displaced or rotated triangular tiling. this ‘map’ is produced by a virtual grid of equilateral triangles that appear to cover the entire surface of the space that the animals are exploring. the path integrator is reset when intermediate stable landmarks occur along a route [12. or if a winner-takes-all system is in operation. however.32]). PI means that the animal integrates internal information about its own self-motion so that it has a continuously upgraded vector of the direction and distance towards home [8. This mechanism is sufficient for birds to reach the wintering quarter and can explain the distribution of wild migrants en route [33].30].25]. could it be that the same underlying set of mechanisms smoothly scales between near and distant space? What the field requires now is bold Current Opinion in Neurobiology 2006. generalize to long distance navigators such as birds? The fact that place cells also occur in the bird hippocampus [41.13] (Figure 1d). it appears that proprioceptive information is more important than optic flow in desert ants [26. research on birds would be the most promising avenue for linking near.42] suggests that this avenue should be explored further in a paradigm that taps into both nearand far-space navigational behavior.29. which are largely derived from studying rodents in a laboratory setting.39] of a spatial map in the entorhinal cortex of rats that contains a directionally oriented and topographically organized neural map of the spatial environment (Figure 1).482 Sensory systems can be used for homing in near-medium distance unknown or rather featureless environments is a form of path integration (PI).19–21. It is not clear whether these various sources are used together and integrated to a final common vector.sciencedirect. But perhaps the most relevant point here is the fact that the tile or grid size increases systematically from the dorsal to the ventral parts of the dorsocaudal medial region of the entorhinal cortex. This leaves us with an intriguing question: do these tessellated triangular grids scale up to kilometers or even thousands of kilometers when an animal has a much larger space to explore and navigate? The fact that these neural maps appear to be anchored to external landmarks in the near-space confines of the test enclosures demonstrates that there has been substantial integration of spatial information at this level. For navigation to or from far unknown space. and simulations show that an animal’s location can be readily derived from population activity levels in the model.31. For example. providing crucial distance information [28]. experiments that bridge the near. If head direction cells and the avian equivalent to entorhinal cortex maps also exist. Considering the obvious conceptual similarities between ‘place cells’ and ‘head direction cells’ on the one hand and maps and compasses on the other. On subsequent journeys along the same route. Compasses After an animal has determined its location relative to some distant goal. animals could use a sequence of local maps to relocate the same routes and/or goals [2. [14. Typically. its next task is to negotiate an efficient route to that goal using compass information that can originate from a variety of sources. such as a virtual reality setup. In an interesting paper that appeared while this article was at the proof stage. a very plausible locally connected neural network model formed on the basis of the activity of dorsocaudal medial entorhinal cortex cells has appeared [40]. For instance. The relative weighting of visual self-motion information probably differs from species to species and from situation to situation. Do these findings. and the neural structures that perform this integration are highly conserved over vertebrate evolution [24. This raises the question of whether more distant landmarks in larger space would also help sew together more detailed local maps (sketch maps) into an animal’s ‘world view’ map (parallel map theory) [11.35]. which involves compasses and an inherited time-program but no map (for a review see [2]). the stars and cues related to the position of the sun (e. Long-distance navigation to an unknown location can also be achieved by navigation mechanisms that do not involve a map.34. Desert ants and many rodents in a variety of laboratory tasks use this strategy when other navigational cues are not available. yet in honey bees optic flow functions as the odometer. Neurobiology of maps Our understanding of near space navigation and its neurobiological substrates has undergone a revolution since the finding of so called ‘place cells’ [36] and ‘head direction cells’ in the rat hippocampus [37.and far-space navigation neurobiology.g. Visual flow is especially relevant because it is processed in (and integrated with) vestibular information. outputs from the vestibular. so animals are almost forced to use cues of a global nature. [18. extrapolation of local cues from the familiar area is no longer likely to provide reliable information. in some species visual flow information from the accessory optic system (or an invertebrate equivalent) might also be involved.23].

sciencedirect.The neural mechanisms of long distance animal navigation Frost and Mouritsen 483 Figure 1 Spatial maps in the brain. which suggested that maps of different spatial resolution vary systematically along the dorsal–ventral axis of the entorhinal cortex. The zones of space where firing rate increases occur are located at the apices of a grid of equilateral triangles that tile the whole space. Warmer colours represent increased firing rates. the location of which is indicated by the black arcs. 16:481–488 . (i) Shows a spatial firing rate pattern produced while a rat explored an arena with a cue card landmark located in the ‘NW’ www. (b) The schematics show that these tesselated grids are anchored to visual landmarks. Cells located more ventrally in this structure have a larger tesselated grid size. (a) Neurons in the dorsocaudal medial entorhinal cortex of rats increase their firing rate at regular intervals as the animal explores a circular experimental Current Opinion in Neurobiology 2006.

this avenue should be explored further. the spectral gradients and/ or even the length and direction of shadows. and that compass information from the sun can also influence the orientation of nocturnal freeflying migrants [45]. the polarization patterns. The central complex then sends information to thoracic motor centers controlling locomotion [47]. such as locusts [47]. little progress has been made in revealing how the visual system specifically processes sun-related compass information. Note that the firing rate map is also rotated by approximately 908. and butterflies [50. Very few velocity tuning curves of AOS neurons in birds have been made.8. whereby axial polarized light is selectively reflected off partitioning membranes of double cones onto ultraviolet sensitive cones.52]. it is crucial to determine which of these features is used. have yet to be determined. if the spatial data obtained with the rotated landmarks are themselves counter-rotated back 908 (i and ii rotated 908) they show a high correlation. such as birds. an ocular structure that is larger and more elaborate in diurnal species that inhabit open places. Because all of these sources of information are tightly correlated with the position of the sun in the sky. for example. the pecten. particularly in highly repetitive environments such as an acacia savanna.51.50]. Interestingly. including. In other words. (ii) shows the rate map for the same neuron when the landmark is rotated 908 into the ‘NE’ sector. which has been associated with the circadian clock in certain species [47. where the local landmark configurations in many locations are very similar. Current Opinion in Neurobiology 2006. Stars Many invertebrates. but how this information is processed centrally. potentially bringing information from the circadian clock into the central complex to provide the ‘time compensation’ required by sun and polarization compasses. However.57]. Polarization [53] and then further processed in the central complex.484 Sensory systems steering towards distant goals in many diurnal species (e. have maps covering a much larger range of scales compared with those reported from rats in the entorhinal cortex.51].48. (c) The graph shows that the spatial correlation between firing rate patterns obtained with the landmark in the initial position (i) and after the 908 landmark rotation (ii) is near zero. the firing patterns of the larger scale maps and/or cells will classify and/or point to the correct one of many similar. (d) Hypothetical figure illustrating how maps of different scale might help animals navigate. which contains homochromatic ommatidia. However. but high between the original firing pattern (i) and the spatial pattern after the landmark was returned to the original position (i’). Figures (a–c) were adapted from [39] using hypothetical data.47]. retinal angular motion produced by stars near the pole star is incredibly slow. but how do birds detect stellar rotation? We suggest that slow visual whole-field rotations are detected by the accessory optic system (AOS). and for most animals it is unknown whether they detect the position of the sun itself. could potentially function as internal sun shade and possibly as an ‘ocular sextant’ ([46]. see Figure 2). spiders [49]. Kenya by H.43. sends axonal connections to the central complex [47]. In locusts (Schistocerca gregaria). can detect polarized light.g. Photograph from Samburu National Park. A very recent study suggests that from the optic lobe this information is integrated with other sources of solar position information Night-migratory birds can use the stars to derive compass information (e. [5. (i’) Shows a firing rate map for the same cell when the landmark is returned to original position. a putative spatial organizer that appears to mediate compass orientation and path integration functions. and ants and bees in particular possess a polarization compass. and even at the stellar equator it will still be only 158 per hour or 0. This local map is represented by neurons the firing patterns of which are connected to more proximate landmarks such as trees and bushes. Insects detect polarization through a specific zone on the dorsal medial margins of their eyes called the dorsal rim area (DRA). Mouritsen. as this will help the search for the sensory mechanism and the parts of the brain that process this information. the differential pattern of sky light intensity. In .g. both for path integration and for finding a direct route home after a foraging trip [8]. Perhaps the exciting work of Homberg and co-workers will soon lead to the discovery of integrative neurons coding sun azimuth and others coding time-compensated geographical direction [53]. Painting over this area abolishes polarization-driven responses in many insects. the processing of e-vector information has been traced from the DRA to the optic lobe [47].44]). In vertebrates.00418 per second. However. These results demonstrate that the firing patterns are anchored to landmarks. Several studies have shown where in the insect brain information from the DRA is subsequently processed. more detailed local scale maps (a process similar to finding the right subdirectory in a computer). a large scale map (here represented by white triangles) connected to prominent landmarks such as hills in the far distance could be used to identify the correct local map to be used (here represented by yellow triangles in the inset on the right). but does not alter migratory sun compass orientation in Monarch butterflies [43]. desert ants and locusts [8. In birds. The categorization performed by the large scale map is likely to be crucial for using the correct local map. the cells of which respond differently to the e-vector of polarized light [8. which the animals can then use for navigation until the large scale map or cells make the animals switch to an adjacent small scale map. it appears to be the square mosaic spatial arrangement of cone photoreceptors that is responsible for this e-vector sensitivity [55]. If animals moving over larger distances. but the two studies that have measured this suggest (by extrapolation) lower limit velocity responses of approximately (Figure 1 Legend continued) sector. and its full behavioral utility. [31]) and they are known to imprint on slowly moving point light patterns to determine the center of rotation and interpret this as ‘north’ [31. the accessory medulla. evidence has accumulated that fish [54] might detect the e-vector of polarized light. Because a similar square mosaic of double cones has been reported in birds [56]. 16:481–488 www. beetles [48].

pleated. e and f are looking directly into the eye along the optic axis with the front of the globe removed). elaborate candidate structure located in the skin of the upper beak. animals could use other parts of the visual system to identify the celestial center of rotation by comparing two or more snapshot images.The neural mechanisms of long distance animal navigation Frost and Mouritsen 485 Figure 2 looked for specifically. The visual streak. and yet a navigational ‘fix’ seems to be what is required. Pecten shadows based on Pettigrew [46]. place the image of the sun on the pecten (or conus papillarus. 16:481–488 The pecten as gnomon or sextant. Magnetic information The magnetic field of the Earth can.61. unpaired electrons) [70] has received strong experimental support as the basis of the magnetic compass of night-migratory songbirds. e and f). because they are probably insensitive to the moderately slow velocity search stimuli used previously. oscillating magnetic fields. Second.71] and covering up the right eye of birds seems to disturb their ability to orient magnetically [72]. the magnetic compass orientation capabilities of European Robins are disturbed by weak. If Pettigrew’s hypotheses are correct then surely one should find neural mechanisms that are particularly sensitive to these shadows and all the useful navigational information they contain. where it would be out of focus and less likely to cause retinal damage. which is a band of high resolution that runs between the centrally located monocular fovea and the temporally located binocular frontal fovea. which is embedded in nerve tissue seemingly as part of the ophthalmic branch of the trigeminal nerve [68]. see a. According to Pettigrew. the magnetic compass of birds and newts is dependent upon the wavelength of light available in the test room [60.20. (e) mid-morning. and thus projects up into the sky.45. when the image of the sun is placed on the retinal periphery the pecten would cast characteristic shadows at various times of . such as birds and many species of lizard. and at the same time position the visual streak on the horizon. the local field strength and/or inclination could provide positional information for use in a map or signpost system.19. But what physiological and molecular mechanisms do the animals use to sense the geomagnetic field? Current evidence suggests that animals can sense geomagnetic information in at least two fundamentally different ways: magnetite-based magnetoreception and chemical (photoreceptor-based) magnetoreception [63. 0. the chimney swallow).63. First. that extends from the optic nerve head down into the ventral retina (See Figure 2a which represents a saggital slice through the eye of a very diurnal. to detect the reference direction provided by the geomagnetic field. and the particular pleat the sun flashed across would provide elevation information and thus constitute and primitive sextant. (d–f) Pecten shadows on the retina of a hudsonian curlew (Numenius hudsonicus) (the pecten structure of which is illustrated in part c). Many different animal species can use geomagnetic cues in the form of a magnetic compass and/or a as magnetic signpost or map sense [18. is assumed to be stabilized on the horizon. Could it be that some diurnal vertebrate species with nearly panoramic vision. and this ability disappears when the ophthalmic branch of the trigeminal nerve is cut [69]. cells with tuning curves specifically adapted to detect celestial rotation might exist in the AOS of night migrating birds. exist in the eyes of migratory birds Current Opinion in Neurobiology 2006. provide two different kinds of useful navigational information. highly vascularized fin (see Figure 2b for details of pleated structure).068/sec [59]. which should not be able to disturb a magnetitebased mechanism [61]. Figure c is redrawn from Wood [76] showing sketch of hudsonian curlew pecten. First. b and c)? The pecten is a heavily pigmented. respectively. and (f) noon are shown in Figure 2 (views d. the cryptochromes. (Figures a and b based on Walls [77]. open sky forager. Alternatively birds could place the image of the sun on the pecten. the direction of the field lines can provide the reference direction for a magnetic compass. Chemical magnetoreception requiring light and being mediated by radical-pair processes (a radical-pair involves two spatially-separated.62–64]. Such cells are likely to go undetected unless www. in principle. Third.60. Hypothetical patterns representing (d) sunrise. who built models to verify these ideas. molecules fulfilling the biophysical characteristics needed for them to function as magnetoreceptors through the radical-pair mechanism. the reptilian precursor.32. It has also been shown that pigeons have a magnetite-rich. But how do the animals detect the geomagnetic cues? Birds [65] and sandhoppers [62] seem to use head scanning movements and whole body scanning movements.66]. Pettigrew [46] proposed that birds could place the image of the sun in the retinal periphery so that the pecten then functions similarly to the gnomon of a sundial to provide explicit patterns of shadows that change systematically with the position and elevation of the sun. The pecten is much larger in diurnal species that inhabit open spaces than in forest dwelling and nocturnal species [76]. the retina and pecten of which are used to illustrate shadows in d.sciencedirect. Furthermore. However. Magnetite-based magnetoreception sensed through the ophthalmic branch of the trigeminal nerve has been demonstrated in fish [67]. Could the pecten be involved in the sun compass of birds? A possible lead that might help the search for neural processing of the sun compass is that direct fixation of the image of the sun on a particular region of the retina is likely to result in retinal damage. This is 10–20 times faster than the rate of stellar equatorial motion. pigeons can be conditioned to a very strong (100. and second. The characteristic 25 Hz eye oscillations of birds would then sweep the image of the sun back and forth across the pecten.0718/sec [58] and 0. Alternatively.000 nT) magnetic anomaly.

Anim Behav 2004. Mouritsen H: Navigation in birds and other animals. spatial maps and the population code for memory. 19:713-731. and J Stalleicken for constructive comments to parts of the manuscript. in the entire forebrain seems to be highly active when night-migratory songbirds perform magnetic orientation at night. Frost BJ: Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms. 99:10162-10166. For a detailed discussion of the magnetic senses in birds and a list of the most crucial open questions. Biegler R: Possible uses of path integration in animal navigation. visual landmarks and cognitive maps. and the University of Oldenburg. In comparison. 15:738-746. Leutgeb S. It will be crucial in future research to investigate whether there are similar structures and mechanisms in animals that navigate over very large distances. animals could have more than one magnetic sense. the VolkswagenStiftung (Nachwuchsgruppe). edn 2. most recent neurobiological progress has been made in identifying the neural mechanisms of compasses that guide animals toward their distant goals. 65:257-272. Cantos FJ. therefore. Piersma T. Curr Opin Neurobiol 2005. Conclusions Thousands of behavioral experiments have demonstrated that many animals are adept at finding their way around the space that constitutes their total habitat. multidisciplinary groups of researchers involving behavioral biologists. In this review. Wiltschko R. Moser MB. Brain Behav Evol 2003. Springer-Verlag. In conclusion. see the review of Mouritsen and Ritz [66]. Anim Behav 2003.63. Anim Learn Behav 2000. These observations suggest that the visual input being processed in cluster N could be light-mediated magnetic compass information. 14. 7. Curr Biol 2004. References and recommended reading Papers of particular interest. Hufford G. 13. Leutgeb JK. In particular. Wiltschko W: Avian navigation: from historical to modern concepts. have been highlighted as:  of special interest  of outstanding interest 1. called Cluster N. By contrast. Mouritsen H: Spatiotemporal orientation strategies of longdistance migrants. the authors examine how path integration information interacts with external landmark based cues. only one cluster of motor-activity-independent brain areas. In the field of long-distance navigation. Telleria JL: Stopover site fidelity of 4 migrant warblers in the Iberian peninsula. 10. they discuss the relationship between activity in place and activity in head direction cells that mediates the internal representation of space.74]. 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Kropp W: Migratory birds use head scans to detect the direction of the earth’s magnetic field. a light-mediated mechanism in the eye(s) of the birds and a magnetite-mediated mechanism in the beak region. Janssen-Bienhold U. Proc Natl Acad Sci USA 2005. The pattern of effects of the oscillating fields is consistent with the expectations from a radical-pair mechanism. Wild JM. albeit indirect. during either the day or the night. Feenders G. which support the suggestion that cryptochromes could be the primary sensor for the magnetic compass in migratory birds. J Exp Biol 2003. 73. The discovery of a seemingly specialized distinct night-vision brain area in night-migratory songbirds supports the idea that they process magnetically modulated visual signals at night. 189:213-220. It remains to be shown that this mechanism can detect biologically relevant magnetic anomalies. 1942. 78. 65.

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