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 (frostb@post.queensu.ca)

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].

Introduction
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
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Maps
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 field.com 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 locusts.sciencedirect.com .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 day.com . 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]. Graham P: Animal navigation: path integration. neurobiologists. Riegen A: Crossing the ultimate ecological barrier: Evidence for an 11000-km-long nonstop flight from Alaska to New Zealand and eastern Australia by Bar-tailed Godwits. In Avian Migration.  Hippocampus 2004. Gwinner E. We believe that major progress in understanding longdistance navigation in animals can be made if larger Current Opinion in Neurobiology 2006. be part of a signpost or map-sense [63. Collett TS. 62:128-139. Jacobs LF. J Comp Physiol A 2003. 2. the radical-pair mediated sense seems to be involved in the magnetic compass only [61. Jeffery KJ: Path integration in mammals.sciencedirect. and the Deutsche Forschungs Gemeinschaft (MO 1408/1-2) (H Mouritsen). 28:257-277. Fourth. All available evidence currently suggests that the magnetite-mediated sense is involved in measuring magnetic field strength and/or inclination angle [21. very little neurobiological progress has been made in unraveling how the sun and star compasses of vertebrates operate. 1998. Because cluster N is inactive in night-migratory birds during the day and seemingly never highly active in non-migratory birds.com . Cluster N seems to be involved in processing some sort of nightvision that seems specialized in night-migratory birds [75]. 15. This work was kindly funded by grants from the Natural sciences and Engineering Research Council of Canada (BJ Frost). published within the annual period of review. 67:189-204. Proc Natl Acad Sci USA 2002. Jacobs LF: The evolution of the cognitive map. 4. Gill RE. molecular biologists and physicists join forces and integrate the concepts of nearand far-space navigation by studying these processes in animals performing both types of tasks. Schenk F: Unpacking the cognitive map: the parallel map theory of hippocampal function. Condor 2005. some significant recent progress has been made regarding magnetodetection in birds. in addition to cells in the dorsocaudal medial region of the entorhinal cortex representing a map-like systematic tiling of space. Laboratory and ‘near’ space studies have shown that place cells and head direction cells in the hippocampus. Sonnenschein E. and the input to this area comes from the eyes [75]. form part of the neuronal substrate for near distance navigation. 11. Servranckx R. and whether similar neural substrates and mechanisms scale up to work also for long-distance navigation. and observable orientation and search behavior. Edited by Berthold P. 14:R475-R477. Image Vis Comput 2001. Wm Caxton Ltd.69] and might. and are located in neurons that are highly active when garden warblers orient magnetically [73]. 9. 3. Moser EI: Place cells. Uruquhart FA: The Monarch Butterfly: International Traveller. 25:131-134.66]. J Avian Biol 1994. Psychol Rev 2003. 5. and they might use these senses for different tasks and/or integrate the information from both senses somewhere in the brain. 8. 2003:493-513. 12. www. 107:1-20. 110:285-315. 189:579-588. 16:481–488 6. In addition. Etienne AS. Acknowledgements We wish to thank S David for preparing the figures. J Gregg for managing the references. 14:180-192. Wallraff HG: Avian olfactory navigation: its empirical  foundation and conceptual state.67. Wehner R: Desert ant navigation: how miniature brains solve complex tasks.66].486 Sensory systems [73. particularly in the case of polarization compasses in the brains of invertebrates. Mouritsen H.

21. Wang JH. 24. J Exp Biol 2004. 188:211-216. 421:60-63. which are directionally and topographically oriented. Moser EI:  Microstructure of a spatial map in the entorhinal cortex. 30. Biol Cybern 2000. 1. Nevitt G.geomagnetic map used in sea-turtle navigation. Muller RU. 207:3537-3544. the lateral accessory lobe and the central complex of the midbrain. Fuhs MC. Vyssotski AL. Bagley DA. Wiltschko R. Boles LC. Lohmann KJ. Tautz J: Honeybee dances communicate distances measured by optic flow. 31. 16. Savini M. projections of the translation zones of the ventral uvula and nodulus. 33. which then controls motor activity. 45. 304:405-408. Dacke M. Zhu HS. but might be offset in phase so that they can. 207:1491-1508. Wikelski M: Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Nature 2001. Dell’Omo G: Pigeon homing along highways and exits. described in the abstract below [53]. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2002. Wiltschko W: Magnetic Orientation in Animals. Muller RU. The author reviews the extensive evidence for the peripheral and central processing mechanisms of polarization vision in insects with a special emphasis on the locust. when modeled. J Theor Biol 2000. Lohmann KJ: True navigation and magnetic maps in spiny lobsters. 188:273-281. 83:261-270. 204:2481-2490. Wylie DRW: A common frame of reference for the analysis of optic flow and vestibular information. Mouritsen O: A mathematical expectation model for bird navigation based on the clock-and-compass strategy. 40. Taube JS. Lohmann CMF. 41. Sci Am 1975. Walker MM.com 36. Science 2004. 15:R171-R173. movement between goals. 10:420-435. Kirschvink JL: The magnetic sense and its use in long-distance navigation by animals. Dacke M. Waxman D: Ant navigation: Reading geometrical signposts. 92:468-471. then through to the anterior optic tubercle. 2. 38. 411:581-583. Wehner R. 1995. Shi DD. 12:707-714. 6:703-712. Casselman A. Taube JS. simulate homing performance similar to that observed in pigeons. This latest work. 42. 428:909-910. Renaudineau S. Neighboring cells have similar spacing and the same orientation. Winship IR. Labhart T. Naturwissenschaften 2005. 39. Zhang S. Sauman I. Molden S. ¨ 48. 47. 190:1047-1062. Navigation and Homing.The neural mechanisms of long distance animal navigation Frost and Mouritsen 487 The utility of olfactory information for pigeon and other bird homing was at one time controversial. Springer-Verlag. Mouritsen H: Do monarch butterflies use polarized skylight for migratory orientation? J Exp Biol 2005. 465:179-194. Wohlgemuth S. Stallelcken J. Reppert SM: Connecting the navigational Current Opinion in Neurobiology 2006. www. 26:4266-4276. Esch HE. 14:1239-1249. lobsters. Frost B. 12:735-744. Etienne AS. Curr Biol 2005. more completely cover the total space of the near environment. Meyer EP: Neural mechanisms in insect navigation: polarization compass and odometer. 208:2399-2408. which. Nitz D. Nevitt GA. 34. 272:17-23. Wylie DRW. Emlen ST: The stellar-orientation system of a migratory bird. but Wallraff reviews the mounting evidence that this sensory modality can play an important role in this behavior. 32. Frost BJ. Curr Opin Neurobiol 2002. Swing T: Animal behaviour . Guilford T: Homing pigeons develop local route stereotypy. 1:303-305. Wallraff shows how gradients and proportional relationships of a number of atmospheric trace compounds can provide map information to these species that is fairly resistant to wind direction. Nat Rev Neurosci 2005. Mouritsen H. Rowe T: Resetting the path integrator: a basic condition for route-based navigation. This region has grid or tile cells that are active whenever the rat crosses any apex of a grid of equilateral triangles that completely tile the whole surface of the near space the animal is exploring. Maurer R. 49. J Neurosci 1990. Proc Roy Soc Lond B Biol Sci 2005. Curr Opin Neurobiol 2002. Pettigrew JD: A role for the avian pecten oculi in orientation to the sun. Warrant EJ: A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle pachysoma striatum. Brown MR. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2004. 15:26-40. 1978:42-54. The author traces polarized vision from specialized photoreceptor cells in the dorsal rim area (DRA) through specific areas in the lamina to the medulla of the optic lobe. 27. therefore. Lohmann KJ: Magnetic orientation and navigation in marine turtles. This study shows that the dorsocaudal medial entorhinal (dMEC) cortex of rats contains neural maps of the near spatial environment. 23.sciencedirect. 16:481–488 . Collett TS. Edited by Schmidt-Koenig K. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2002. the author suggests that polarized light information might be integrated with information on solar position by work that will appear in publication very soon. 45:539-546. Johnsen S. Ehrhart LM. 37. 91:199-208. reminiscent of orientation columns in the visual cortex of mammals. Stalleicken J. J Neurosci 1990. Ronacher B. Hafting T. Reid K. Mouritsen H. Moser MB. 44:121-140. 20. Labhart T. there appears to be a systematic representation of scale from more dorsal towards more ventral loci in the dMEC. Wehner R: Vector navigation in desert ants. Integr Comp Biol 2005. 17. J Exp Biol 2001. Srinivasan MV. Cain SD. Yuan Q. Moreover. will demonstrate that sun azimuthal position. 26. Biology Letters 2005. 50. Wehner R: Distance estimation in the third dimension in desert ants. 18. Froy O. This might enable animals to move from one part of their larger environment to another and then retrieve the local sketch maps relative to their current location (Figure 1d). Boles LC. and molluscs: concepts and conundrums. Cochran WW. Lipp HP. Boulens V. An excellent review of the theoretical and physical background and key behavioral and neurobiological evidence for magnetoreception. 25. Hippocampus 2005. Exp Neurol 1976. J Exp Biol 2004. 207:283-291. Springer-Verlag. In Animal Migration. Int Rev Neurobiol 2000. and environmental context in a radial-arm arena. Most intriguingly. Cataglyphis fortis: celestial compass cues are essential for the proper use of distance information. 233:102-111. Biro D. Mukhida M. Detailed gas chromatographic analyses data reveal that differentially oriented gradients of volatile hydrocarbons exist. ¨ Troster G. Lohmann KJ: The physics and neurobiology of  magnetoreception. Touretzky DS: A spin glass model of path integration in rat medial entorhinal cortex. Ranck JB: Head-direction cells recorded from the postsubiculum in freely moving rats. 35. Homberg U: In search of the sky compass in the insect brain. Hough GE. Meade J. J Comp Neurol 2003. These maps are anchored to conspicuous nearby landmarks. 29. Nature 2003. Nature 2004. Briscoe AD. Nordstrom P. 19. polarization patterns and perhaps even gradients of spectral distribution in the sky are all integrated together in the central complex. 44. effects of environmental manipulations. Todd KG: Zonal organization of the vestibulocerebellum in pigeons (columba livia): III. Scholtz CH. O’Carroll DC: Polarized light detection in spiders. O’Keefe J: Place units in the hippocampus of the freely moving rat. 436:801-806. Bingman VP: Spatial response properties of homing pigeon hippocampal neurons: correlations with goal locations. Dennis TE. 43. Mittelstaedt H: Triple-loop model of path control by head direction and place cells.  Naturwissenschaften 2004. Wolfer DP. Ranck JB: Head-direction cells recorded from the postsubiculum in freely moving rats. J Neurosci 2006. Nature 2005. Crowder NA. 51:78-109. Levy A. Trathan P: Testing olfactory foraging strategies in an antarctic seabird assemblage. Fyhn M. 10:436-447. description and quantitative-analysis. Moreover. 28. Bingman VP: Spatial-specificity of single-units in the hippocampal formation of freely moving homing pigeons. Siegel JJ. Schistocerca gergaria. Bonadonna F: Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. 22. Curr Biol 2004. Doan TA. coauthored by one of the main contributors to the field of magnetic navigation and magnetoreception. 46. Sommer S.

They summarize the review by listing 10 of the most crucial open questions currently facing researchers studying magnetoreception in birds and other animals. Petersen N. show high levels of neuronal activity during magnetic orientation in migratory birds. Adem S. ¨ 68. These results represent the strongest currently available. Morgan B. a putative magnetoreceptive molecule. The authors demonstrate that cryptochromes. The authors use sensory-driven gene expression to show that night migratory songbirds possess a tight cluster of brain regions. 77. Philos Trans R Soc Lond B Biol Sci 2000. The authors use operant conditioning to show that pigeons can detect a strong (100. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2003. 62. Crowder NA. Wada K. Mora CV. Wiltschko W. Proc Natl Acad Sci USA 2004. a putative magnetoreceptive molecule. 47:368-379. ‘Cluster N’. 218. 419:467-470. The authors review the evidence for magnetoreception in birds. 55. Diebel CE. J Neurophysiol 2003. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2006.neuro. and they map the cellular location of cryptochromes within the retina. Cain SD. 67. Fleissner G. Montgomery JC: Structure and function of the vertebrate magnetic sense. Mouritsen H. Hanzlik M. Wylie DRW: Temporal frequency and velocity-like tuning in the pigeon accessory optic system. Fleissner G. the European Robin. are found in the retinae of night-migratory garden warblers. Thalau P. Meyer EP: Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. 66. are found in the retina of a night-migratory bird. 52. Homberg U: Integration of celestial orientation cues in an identified neuron in the brain of the desert locust schistocerca gregaria. Available online: www. 51. Phillips JB. Wang JH. Walls GL: The Vertebrate Eye and its Adaptive Radiation. Wiltschko W: Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. Semm P: Does the avian ophthalmic nerve carry magnetic navigational information? J Exp Biol 1996. Walker MM. Phillips JB. Wiltschko R: Lightdependent magnetoreception in birds: interaction of at least two different receptors. Wiltschko W. Naturwissenschaften 2002. The authors show that cryptochromes. sylvia borin. Jarvis ED:  Night-vision brain area in migratory songbirds. Davison M. 14:1946-1949. Wiltschko W:  Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Schierwater B: Retinal  cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. 64. 429:177-180. Holtkamp-Rotzler E. Sagasser S. Naturwissenschaften 2004. Feenders G. 61. Stalleicken J. Liedvogel M. J Comp Neurol 1970. Frost BJ: Visual response characteristics of neurons in nucleus of basal optic root of pigeons. Nature 2004. Microsc Res Tech 1999. Ethology 1987. Wiltschko R: Lateralization of magnetic compass orientation in a migratory bird. Hawryshyn CW: Ultraviolet polarization vision in fishes: possible mechanisms for coding e-vector. 90:1829-1841. Liedvogel M. Moyer HD. Biophys J 2000. 74:285-292. Nature 1992. 54. Wiltschko W. Nature 2004. Hawryshyn CW. Ritz T. 46:457-467. but cannot easily be reconciled with other mechanisms. 355:1187-1190. Gesson M. Gunturkun O. 76. Feenders G. Mouritsen H. Haimberger TJ. Dirks P. 70.de/archiv/2005/pdf/ Proceedings-Goettingen2005. Liedvogel M. Morris VB: Symmetry in a receptor mosaic demonstrated in the chick from the frequencies. 458:350-360. 75. McFarland WN: Multidimensional polarization sensitivity in damselfishes. Labhart T.  Stalleicken J.sciencedirect. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2006. 1917. Prior H. Naturwissenschaften 2004. Daum P. The Lakeside Press. Mouritsen H. 390:371-373. spacing and arrangement of the types of retinal receptor. Fergenbauer-Kimmel A. 89:445-452. 59. 140:359-398. 101:14294-14299. 71. Curr Biol 2004. Wiltschko R: The development of the star compass in garden warblers.com . 91:585-588. Ugolini A: Equatorial sandhoppers use body scans to detect the earth’s magnetic field. Nature 1997. 63. Walker MM: Magnetoreception  and its trigeminal mediation in the homing pigeon. Pfeiffer K. ¨ 74. 192:321-331. Wiltschko R: Magnetic compass orientation in birds and its physiological basis. They conclude that birds probably possess two different magnetoreception mechanisms. 2005. Current Opinion in Neurobiology 2006. Furthermore. Weiler R: Cryptochromes and neuronalactivity markers colocalize in the retina of migratory birds during magnetic orientation. Wiltschko W. Traudt J. Beason RC. Older results of Beason and Semm [78] suggest that magnetic information transmitted through the trigeminal nerve is not needed for magnetic compass orientation. 69. 56.488 Sensory systems clock to sun compass input in monarch butterfly brain. Kinoshita M. 15:406-414. 199:1241-1244. Wiltschko W. Proceedings of the 6th Meeting of the German Neuroscience Society. 16:481–488 www.000 nanoTesla) magnetic anomaly and that the ophthalmic branch of the trigeminal nerve carries this magnetic information to the brain. Hafner. Haugh CV. 359:142-144. Ritz T. 72. 60. Lohmann KJ: Identification of magnetically responsive neurons in the marine mollusc Tritonia diomedea. 102:8339-8344. 432:508-511. Wiltschko R.uni-goettingen. Dawson MRW. 192:45-49. neuronal activation of Cluster N was not increased in nonmigratory birds. Winklhofer M. 42:181-188. that are highly active only during night-vision. The authors also show that the retinal ganglion cells and displaced ganglion cells. evidence for a chemical magnetodetection mechanism in birds. Schulten K: A model for photoreceptor-based magnetoreception in birds. Moller A. Wood CA: The Fundus Oculi of Birds. Borland SC: Behavioral evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Stapput K. which also contain lots of cryptochrome. Allison WT. Ritz T: Magnetoreception and its use in bird  navigation. Mouritsen H. Pankhurst PM. Curr Opin Neurobiol 2005. 206:381-388. 53. 78:707-718.pdf. Neuron 2005. Mouritsen H: Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. Exp Brain Res 1981. J Comp Neurol 2003. the authors found clear differences in cryptochrome expression and neuronal activity between migratory garden warblers and non-migratory zebra finches. No increase in activity in Cluster N was observed during the day in any birds and the activity in Cluster N disappeared in migrants when both eyes were covered. Labhart T. Nature 2002. 57. The authors show that 470 nT oscillating magnetic fields in the low radiofrequency range disrupt the magnetic compass responses of migratory birds. 91:130-134. By contrast. 58. 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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