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Animal Navigation: A Map for All the direction in which the animals attempt to move is measured. With Seasons nothing more to go on than the two magnetic-field parameters, the creatures attempt to home to their Before migrating from their home streams to the ocean, young Pacific salmon apparent point of capture; all other already know the magnetic parameters of their feeding grounds, allowing them potential locational cues at the testing to steer into a favorable habitat. What kind of ‘map’ representation underlies site are unchanged, and necessarily this remarkable ability? inappropriate for the false position the animals apparently infer for James L. Gould incompatible navigational strategies be themselves. Titration of the arbitrary reconciled? redeployment distances in these virtual ‘True’ navigation is the ability of an A series of telling anomalies displacements suggests, again, an animal to travel to a relatively precise suggested more than 30 years ago that accuracy of a few kilometers [8]. target at a considerable distance the map sense of mature pigeons is But homing is only a part of without the need for familiar landmarks based in large part on measuring the map-based orientation. Most species [1]. To do this, the navigator must total strength and inclination of the apparently do not home reliably normally have a ‘map’ to show where it earth’s magnetic field at the release site (though we may have failed to look is relative to its goal. Having inferred and then comparing those parameters carefully enough). Seasonal migration the direction to the target from this with the values at the home loft [4,5]. seems far more common but is map, the organism then needs a Under special circumstances, pigeons experimentally less amenable. The task compass to steer itself along the may be able to use odors [1], acoustic for most first-time migrants is daunting: appropriate vector. A great deal is beacons [6], or other cues. To use a birds, for instance, typically fly alone known about the various redundant bicoordinate magnetic map, the bird and at night along an innate vector (or a and self-calibrating compasses, used must not only have measured the series of vectors) until they reach their interchangeably or hierarchically as absolute values of the two components destinations [1]. In some dramatic circumstances and the animal’s at the loft, but more importantly, the cases, the target is highly isolated — for experience dictate [1]. The ‘map sense’ direction and rate of change of their example, one population of the has been more controversial and less gradients. This would permit the animal bristle-thighed curlew, a shorebird, amenable to experimentation. A new to extrapolate from its limited home travels from a small home range in paper in this issue of Current Biology range to distant release sites, infer its Alaska to the Marshall Islands, mere by Putman et al. [2] adds significantly to own location and set course home. specks in the vast Pacific Ocean, our understanding of the map sense, Learning (or calibration) is essential. requiring a nonstop, seven-day journey but now forces us to ask just what we That animals might utilize magnetic of 8,500 kilometers [11]. Without some mean by ‘map’, and whether animals cues, to which we are entirely blind, sort of map for at least the last part of may have multiple map senses or measure gradients to a better accuracy the odyssey, the task seems hopeless. representations. than portable human technology could For most species, however, the target The thinking about animal maps (at least until recently), and employ a (the winter or summer range) is so has been largely shaped by work on non-orthogonal set of coordinates to large that no map sense would seem pigeons that home to an imprinted loft place themselves accurately even necessary — a flight vector and a way location rather than migrating between hundreds of kilometers away, seems to judge latitude should be sufficient. winter and summer ranges. This makes fantastic. Equally incredible is the And yet, when birds are intercepted homing pigeons a convenient model inferred precision of the pigeon map, en route and displaced hundreds or system, but it’s important to keep in based on how close visually impaired thousands of kilometers in longitude, mind that they are homers rather than birds get to their loft after homing: those who have made the journey at migrants; nor do they have a single map about 5 kilometers [7]. But, as usual, a least once before appear to recognize algorithm: homing requires flying shortfall in human imagination does not that their previous route is now useless, experience near the loft and matures seem to have limited the potential of and accurately reorient their flight between about 6 weeks (fledging) and natural selection to fashion solutions to paths from a location never before 12 weeks of age, during which time the life-or-death challenges. encountered along a vector never gathering and processing of map The proof that magnetic cues alone before flown [12,13]. That first-time information (and the use of compasses) are sufficient to allow accurate migrants cannot use their map under changes dramatically [1]. Researchers map-like responses came with work on these conditions implies that the typically imagine that animals create, mature newts [8], spiny lobsters [9], essential calibration for wide-area calibrate, and utilize the kind of and sea turtles [10]. The approach used positioning must occur during or at the two-dimensional graphic charts we call for such studies is elegant and end of the initial journey. maps, but the juvenile salmon (Figure 1) well-controlled: the animals are A change in the use of some sort of tested by Putman et al. [2] (and, in captured and tested nearby in a map with experience is also evident in retrospect, his hatchling sea turtles in chamber enclosed by coils that both salmon [3] and sea turtles [2]. The earlier work [3]) appear to have generate a magnetic field, the strength initial task for the young is to stay within something like an innate look-up table and inclination angle of which is set to a broad home area — the feeding which requires no prior experience or be characteristic of a location dozens grounds for Chinook salmon in the calibration. Can these two seemingly or hundreds of kilometers away. Then, North Pacific, the foraging range for Current Biology Vol 24 No 4 R154

turtles? Titration tests might reveal surprising hidden precision. How do creatures manage in the small regions of the globe when the gradients of intensity and inclination are parallel? Do they resort to other cues, or interpolate from adjacent areas? And how can it be that the orientation of homers actually improves the farther away they are displaced? The map sense remains animal behaviour’s mystery of mysteries. No other set of questions takes us so far from human experience and analogy. The phenomena continue to require almost impossible leaps of imagination to formulate hypotheses, much less to devise practicable controlled tests. Even when successful, we are generally treated to isolated episodes in the navigational life of one kind of animal or another. The study by Putman et al. [2], Figure 1. Juvenile Chinook salmon. brings us much closer to an integrated Salmon fry develop quickly in their home streams into parr (shown here). A few months later picture from birth to death of a single most of the parrs transform into smolts, undergo the physiological changes that will permit species — its receptor systems [16], them to survive in salt water, and begin migrating downstream to the ocean. After travelling juvenile migration, and adult homing up to hundreds of kilometers to reach the sea, they must then make their way to the feeding grounds. The adults return to their natal streams a few years later to breed (photo: Tom Quinn [17]. It also reminds us that the best and Richard Bell). questions are now ready to be attacked. turtles in the North Atlantic gyre. Given until they get within range of this spot or References the geographical extent of these region — an ‘I’ll-know-it-when-I-get- 1. Gould, J.L., and Gould, C.G. (2012). Nature’s Compass: The Mystery of Animal Navigation targets, the orientation seems to imply close’ strategy. With experience, (Princeton: Princeton University Press). at a minimum only a low-resolution though, many creatures develop an 2. Putman, N.F., Scanlan, M.M., Billman, E.J., map or a simple look-up table — a ability to use their map algorithm over O’Neil, J.P., Couture, R.B., Quinn, T.P., Lohmann, K.J., and Noakes, D.L.G. (2014). An listing of pairs of magnetic parameters ever-greater distances. inherited magnetic map guides ocean (total intensity and inclination) and the But what sort of maps are these? Are navigation in juvenile Pacific salmon. Curr. Biol. 24, 446–450. appropriate directional response for the map-like representations used in 3. Putman, N.F., Endres, C.S., Lohmann, C.M.F., each. But there must be more, since homing versus migration the same and Lohmann, K.J. (2011). Longitude later the members of both species (with task-specific algorithms) or are perception and bicoordinate magnetic maps in sea turtles. Curr. Biol. 21, 463–466. return with pinpoint accuracy to the they organized along different lines 4. Gould, J.L. (1980). The case for magnetic natal river or beach to breed. The altogether? Are the maps truly global, sensitivity in birds and bees. Am. Sci. 68,256–267. 5. Gould, J.L. (1982). The map sense of pigeons. measurements needed for the more as the frequent references to an ‘animal Nature 296, 205–211. demanding adult navigational feats are GPS’ suggest [14]? Or are they 6. Hagstrum, J.T. (2013). Atmospheric necessarily made very early on when centered on the goal, filled in with propagation modeling indicates homing pigeons use loft-specific infrasonic ‘‘map’’ they imprint on their natal beach/river experience? Or, more likely, are there cues. J. Exp. Biol. 216, 687–699. mouth, well before the animals must two wide-area maps, one for each end 7. Schmidt-Koenig, K., and Walcott, C. (1978). Tracks of pigeon homing with frosted lenses. locate their respective feeding ranges. of the annual trip? Are these maps Anim. Behav. 26, 480–486. Definitions and generalizations special-purpose creations or ever- 8. Phillips, J.B., Freake, M.J., Fischer, J.H., and are inevitably human simplifications, evolving multimodal wonders like the Borland, S.C. (2002). Behavioral titration of a magnetic map coordinate. J. Comp. Physiol. A rather than constraints on reality. place-cell-based hippocampal maps of 188, 157–160. Nevertheless, surveying birds, reptiles, mammals? [15] Or are the maps 9. Boles, L.C., and Lohmann, K.J. (2003). True navigation and magnetic maps in spiny amphibians, and now fish, a few analogous to Excel tables — lists of lobsters. Nature 421, 60–63. general patterns seem to be emerging. magnetic coordinates with the 10. Lohmann, K.J., Lohmann, C.M.F., Ehrhart, L.M., Among species that make use of a map seasonally appropriate directional Bagley, D.A., and Swing, K. (2004). Geomagnetic map used in sea turtle navigation. sense, for instance, the positional responses filled in, perhaps innate Nature 428, 909. information and processing seem initially but revised with learning and 11. McCaffery, B.J. (2008). On scimitar wings. Birding 40, 50–59. to mature or evolve with time or calibration? These new results 12. Thorup, K., Bisson, I.A., Bowlin, M.S., experience. Many species — the young implying, at least naively, a low- Holland, R.A., Wingfield, J.C., Ramenofsky, R., salmon and turtles as well as first-time resolution look-up table pose other and Wikelski, M. (2007). Evidence for a navigational map stretching across the migrants — appear to have an innate intriguing and important questions as continental U.S. in a migratory songbird. Proc. target, large or small as selection has well. What, in fact, is the distance Natl. Acad. Sci. USA 104, 181155–181159. 13. Chernetsov, N., Kishkinev, D., and dictated. 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displacement during spring migration. Curr. 16. Walker, M.M., Diebel, C.E., Haugh, C.V., Department of Ecology and Evolutionary Biol. 18, 188–190. Pankhurst, P.M., Montgomery, J.C., and Biology, Princeton University, Princeton, 14. Lohmann, K.J., Lohmann, C.M.F., and Green, C.R. (1997). Structure and function of the NJ 08544-1003, USA. Putman, N.F. (2007). Magnetic maps in animals: vertebrate magnetic sense. Nature 390, 371–376. nature’s GPS. J. Exp. Biol. 210, 3697–3705. 17. Putman, N.F., Lohmann, K.J., Putman, E.M., E-mail: [email protected] 15. Jacobs, L.F., and Schenk, F. (2003). Unpacking Klimley, A.P., Quinn, T.P., and Noakes, D.L.G. the cognitive map: the parallel map theory of (2013). Evidence for geomagnetic imprinting as hippocampal function. Psychol. Rev. 110, a homing mechanism in Pacific salmon. Curr. 285–315. Biol. 23, 312–316. http://dx.doi.org/10.1016/j.cub.2014.01.030

Visual Circuits: Mouse Retina No representation of the central, binocular field of view. Longer a Level Playing Field Previous work explored cell densities across the mouse retina and found that RGCs exhibit a modest two-fold Unlike humans, monkeys, or carnivores, mice are thought to lack a retinal reduction in density from center to subregion devoted to high-resolution vision; systematic analysis has now periphery [6,7]. However, such studies shown that mice encode visual space non-uniformly, increasing their spatial considered RGCs as a singular sampling of the binocular visual field. population and did not distinguish among the two-dozen or so RGC Onkar S. Dhande Non-uniform mapping is a subtypes that exist in this species [9]. and Andrew D. Huberman well-established feature of primate In their study, Bleckert et al. [1] and carnivore visual circuits; the combined molecular markers and Our brains evolved to accurately photoreceptors and the neurons that electrophysiological characterization represent the world around us. This signal visual information to the brain, of alpha-RGCs to reliably identify process begins with the sense organs: the retinal ganglion cells (RGC), are far these cells. By meticulously surveying the skin, eyes, ears, mouth and nose. more numerous in the central as the distribution and dendritic size Thus, just as knowledge about the compared to the peripheral retina [4]. of one subtype of alpha-RGCs, type and density of pixels in a digital This dependence of RGC density On-sustained alpha or ‘Aon-s’ camera will tell you a lot about the on distance from the central retina, RGCs, as a function of eccentricity and quality of images that the camera will or ‘eccentricity’, is propagated to retinal quadrant, they discovered that take — monochrome versus color, higher visual processing centers in Aon-s RGCs are much more numerous low versus high resolution, and so the brain and has profound and densely packed within the on — knowing the type and layout consequences on the spatial acuity temporal retina. They also found that of receptors harbored within the when viewing central versus peripheral temporal Aon-s RGCs accomplish this sense organs is crucial for understand space. because their dendritic arbors are sensory processing. In a recent As the mouse has become an much smaller than those of nasal Aon-s issue of Current Biology, Bleckert increasingly popular model for RGCs. et al. [1] report an unexpected studies of visual processing over In primates, the increase in distribution of a specific subtype of the last decade [5], it has become RGC density towards the fovea is visual receptors in the mouse eye, crucial to determine if and how accompanied by a decrease in the raising the question: what does a their visual systems differ from that of convergence of cells that provide input mouse see? more traditionally studied model to them, such as bipolar cells. The net A common feature among the species such as cats and monkeys. result is increased spatial sampling of various sensory modalities is One key difference is that the the visual scene in the fovea [4,8]. topographic mapping whereby mouse lacks a steep eccentricity Bleckert et al. [1] asked whether this neighboring receptors are represented gradient of photoreceptors or was also the case in the mouse. A by neighboring sets of neurons in the RGCs [6,7] and hence its visual systematic measurement of the bipolar brain [2]. Despite this point-to-point system is thought to encode all neurons that provide excitatory inputs organization, the geometry of points in visual space relatively to Aon-s RGCs revealed that their these maps is by no means uniformly. Bleckert et al. [1] report distribution and axonal size was uniform. For example, our fingertips the surprising finding that not all unchanged across the retina. Thus, in contain a denser collection of subtypes of mouse RGCs contrast to the primate fovea, these touch receptors and more cortical are uniformly arrayed across the data suggest that in the mouse, the area is devoted to them, relative retina. They show that a well-known eccentricity gradients of different to the cortical representation of type of RGC called the alpha cell [4,8] retinal neurons (such as RGCs, bipolar body regions such as the back, exhibits dramatic variation in size cells, photoreceptors) are not yoked to which is less sensitive. Indeed, and density according to position each other. this biased representation is evident along the nasal-to-temporal retinal Generally, the dendritic arbor size in our ability to discern smaller axis. From the overall layout of of a RGC closely matches its separations of contact on our these gradients in the two eyes, the receptive field size [10]. Surprisingly, fingertips as compared to on our data suggest that such variation may Bleckert et al. [1] also found that, torso [3]. afford the mouse an enhanced whereas the dendritic and receptive