Exploration Is Sufficient but Not Necessary for Navigation with Landmarks in the House Mouse (Mus musculus)

LEARNING AND MOTIVATION ARTICLE NO.

28, 558–576 (1997)

LM970985

Exploration Is Sufficient but Not Necessary for Navigation with Landmarks in the House Mouse (Mus musculus) Sofyan Alyan Department of Systematics and Ecology, University of Kansas

and Rudolf Jander Department of Systematics and Ecology and Department of Entomology, University of Kansas Exploration is a locomotor and scanning behavior accompanied by the acquisition of information that can be used for topographic orientation and homing. Our experiments demonstrate that the exploring house mouse (Mus musculus) learns the use of distal landmarks for short-range homing. However, mice that had no exploratory experience at all also learned how to use distal landmarks for homing while shuttling between two goals. In addition, exploration-based knowledge in itself appears to be weak or provisional. Whereas one straight line path integration is strong enough to override orientation by distal landmarks based on 1 day of exploration, prolonged straight line shuttling results in navigation by distal landmarks that is strong enough to override path integration based on prolonged straight line shuttling. We conclude that exploratory behavior by itself is sufficient, but not necessary, for learning the use of distal landmarks for navigation within the home range. q 1997 Academic Press

House mice (Mus musculus, Berry & Bronson, 1992; Boursot, Auffray, Britton-Davidan, & Bonhomme, 1993), like all vertebrates, explore their environment by locomotion and inspection of objects. ‘‘Exploration’’ will be defined as the whole collection of apparently undirected behaviors including movement through space, rearing, sniffing, location changes, etc. (Renner & Seltzer, 1991). Novel environments incite exploration, which, in turn, reduces

We are greatly indebted to Lynn Nadel and Ariane S. Etienne, whose critique of, and comments on, an earlier draft helped us in making clear many of the ideas presented in this article. We also thank Dr. Bennet G. Galef, Jr., and two anonymous reviewers for making valuable suggestions. Address correspondence and reprint requests to Rudolf Jander, Dept. of Systematics and Ecology, University of Kansas, Lawrence, KS 66045. 558 0023-9690/97 $25.00 Copyright q 1997 by Academic Press All rights of reproduction in any form reserved.

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the novelty of the traversed environment (Archer & Birke, 1983; Voss & Keller, 1986; Renner 1990; Thinus-Blanc, Save, Buhot, & Poucet, 1991). Novelty is defined in terms of the subject’s behavior: any change in a thoroughly familiar environment that incites exploration. It has been known for over half a century that novelty is a sufficient incentive for exploratory learning and that spatially distributed rewards and punishments (i.e., reinforcement) are not required (Blodgett, 1929; Tolman & Honzik, 1930b; Berlyne, 1958; O’Keefe & Nadel, 1978). Hence, exploration is classified as a form of latent learning (Blodgett, 1929; Mackintosh, 1974; Honig, 1987). Exploratory locomotion of a rodent normally originates from a privileged location, such as a shelter, nest, or den (Barnett, 1958; Ewer, 1967; Eilam & Golani, 1989). Because the exploring rodent regularly returns to and departs from such a location, we will refer to it as the ‘‘anchor’’ of exploratory activity. As exploration proceeds and expands, secondary anchors may develop, or one anchor may be replaced by another. Familiarity due to exploration implies the acquisition of some knowledge about the environment (Renner, 1988; Renner & Rosenweig, 1986). Many questions about the nature and use of this knowledge in rodents are still open, even though the exploratory behavior of rodents has been better investigated than that of any other vertebrate (Honig, 1987; Thinus-Blanc et al., 1991). Our research was prompted by the following three findings that were difficult to reconcile within a unified theory of rodent exploration. First, it is well known that exploring rodents are strongly attracted to novel proximal objects or landmarks, and novel proximal object constellations, which they investigate and thereby become familiar with (Berlyne, 1950; Shillito, 1963; Brown, 1966; Croman & Shafer, 1968; Sales, 1968; Wilz & Bolton, 1971; Barnett & Smart, 1975; Cowan, 1976, 1983; Cheal, 1978; Poucet, Chapius, Durup, & Thinus-Blanc, 1986; Thinus-Blanc, Chapius, Bouzuba, Durup, & Poucet, 1987, Thinus-Blanc et al., 1991; Ennaceur & Delacour, 1988; Roullet & Lasalle, 1990; Xavier et al., 1991; Alyan & Jander, 1994). This will be referred to as ‘‘investigation,’’ following Renner & Seltzer (1991). In contrast to the pronounced responding to proximal objects or landmarks during investigation, rodents preferentially refer to distal landmarks when performing reinforced goal directed locomotion; proximal objects, apparently, are ignored in this process (Hebb, 1949; Olton, 1979; Olton & Samuelson, 1976; Suzuki, Augerinos, & Black, 1980; Sutherland & Dyck, 1984; Best & Thompson, 1989; Alyan & Jander, 1994). There is a consensus that distal landmarks, if available, are the preferred cues of orientation for rodents navigating in open spaces (Alyan & Jander, 1994; Etienne, Teroni, Hurni, & Portenier, 1990; Munn, 1950; O’Keefe & Nadel, 1978; Olton, 1979; Restle, 1957; Schenk, 1985). Second, although distal landmarks are preferred over proximal ones as for use in orientation, we found that in mice, navigation by distal cues develops a posteriori, after the mice had oriented by means of path integration (Alyan &

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Jander, 1994). When, after extensive investigation and exploration, house mice learn how to home from a distance of 50 cm, they first rely on path integration and only thereafter on distal landmarks. Path integration is defined as the continuous monitoring of spatial displacements combined with computation of the locomotor vector to the starting point of the path. Landmark navigation implies the use of distal visual cues to move toward a goal that is not directly perceived. Path integration differs from landmark navigation in the absence of place recognition, except for the one or several points in space to which path integration is anchored (Alyan & Jander, 1994). Thus, it is conceivable that in a novel environment house mice and other rodents first explore to get acquainted with proximal landmarks, then navigate to some goal of interest by means of path integration, and finally acquire and preferentially use the skill of navigating by means of distal landmarks. Third, the hypothetical topographical learning sequence just mentioned— investigate proximal objects, then first learn to approach a goal by path integration and then by distal landmarks—is inconsistent with the observation that in rodents exploration facilitates the subsequent learning of goal directed navigation (Blodgett, 1929; Tolman & Honzik, 1930b; Ellen, Parko, Wages, Doherty, & Herrmann, 1982; Thinus-Blanc et al., 1991). This facilitation could be due to some exploratory learning about proximal landmarks or about distal landmarks, or about both. Indeed, there is evidence that during exploration some spatial relations between distal landmarks are learned and used thereafter in goal directed navigation (Tolman & Honzik, 1930a; Ellen et al., 1982; Sutherland & Dyck, 1984; Chamizo & Mackintosh, 1989; Whishaw, 1991). Why then do mice that learn to navigate between two goals first rely on path integration and only later, after more experience, on distal visual landmarks (Alyan & Jander, 1994)? In order to resolve this problem — the first task in this study — we attempted to answer the question: is exploration necessary in order for the mouse to learn landmark-based navigation between two goals? In the context of this task, questions of motivation come into play. In all our experiments we motivated female mice to shuttle between two goals by placing their pups outside the nest to be retrieved. It is known that intensely exploring mice make few attempts at retrieving pups into the nest (Barnett & Fraser, 1950; repeatedly confirmed by our observations). This failure to retrieve while exploring can be due to either motivational suppression of retrieval by curiosity or fear or to the need to first learn about the home range by free exploration in order to home successfully and efficiently. Indeed, it is well known that exploratory curiosity or associated fear can dominate over other drives such as hunger (Rabinovitch & Rosvold, 1951; Hebb & Mahut, 1955; Havelka, 1956; Berlyne, 1958, 1966). To resolve this motivational problem we suppressed all free exploration in a novel environment by strongly inciting the mice to learn shuttling between points. This allowed us to test for incidental learning of the distal

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landmarks by mice that lacked exploratory experience. These mice had to learn to use distal cues while shuttling between two goals. In the second task of this study, we investigated the hypothesis that the exploring mouse initially uses learned landmark representation of the spatial relationships between distal landmarks provisionally. At this provisional stage, the mice would rely more on path integration to go back home. Thereafter, when thoroughly learning to navigate home from one particular location, the mouse representation of distal landmarks gets stronger and overtakes directing homing trajectories. GENERAL METHODS

Animals Pigmented laboratory female house mice (Mus musculus) were used. Prior to experimentation they were housed in transparent cages 25 1 50 cm. The floor was covered with wood shavings, and food and water were provided ad libitum all the time. The photoperiod was 12:12 h (dark 7:00 pm to 7:00 am) and all the experiments were conducted between 10:00 am and 2:00 pm. It is in our experience that mice perform equally well whether they were tested in the light vs dark cycle. Each individual mouse was used only once for one trial in one experiment to assure independence of all trials and experiments. That is, all animals were experimentally naive. Arena and Surroundings Two circular arenas, 1 m in diameter each, were used. The floor of each was covered with a layer of sand, 2 cm deep, that was mixed between tests in order to disperse local odor cues. Their edges were fenced off to a height of 10 cm by sheet metal painted black on the inside and then to a height of 40 cm by Plexiglas. A hole in the fence just above the sandy floor gave access to a nest located directly outside each arena. Shredded brown paper towel was used as nesting material. Each arena rested on ball-point bearings, permitting rapid rotation by means of handle bars on the outside. The experimental room was normally lit from the ceiling by standard florescent tubes. To suppress access to extra-arena cues in some experiments, the experimental room was fully darkened except for a central 40 watt incandescent overhead spot light which selectively illuminated the inside of the arena, leaving the outside in dark shade. In addition, a dark-tinted sheet surrounded the Plexiglas fence establishing one-way viewing from the outside. Training, Testing, and Data Analysis In all experiments the mice retrieved their pups from the center of the experimental arena into the nest. Prior to testing directional choices, the arenas were rotated 907, either clockwise or counterclockwise. The purpose of such rotation was to separate

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the use made by the mouse of intra-arena cues, of path integration, and of distal visual landmarks, depending on additional experimental manipulations to be specified for each experiment. The reported directions taken by the mice at the final return runs under test conditions were all related to the extra-arena environment. The azimuth (07) direction is always the direction to which all homing mice had been trained, and the 907 direction is the direction to which the arena had been rotated relative to the environment prior to testing, irrespective of whether this rotation was clockwise or counterclockwise. All directional measurements were analyzed using circular statistics (Batschelet, 1981; Cabrera, SchmidtKoenig, Watson, 1991; Zar, 1996). In addition, linear statistics were used in cases where no probability values could be obtained using circular statistics, in particular to calculate the 99% confidence interval for small sample sizes. The directional measurements were clustered enough to justify the use of linear statistics in all cases. Although linear statistics yielded the same results as the circular statistics, we preferred the use of circular statistics since our data were directional in nature. For each sample, the following parameters were used in evaluating the homing performance of the mice. A sample analysis yields a mean vector, m. This m is defined by its polar coordinates: Ø and r, where Ø is the sample mean direction and r is the length of m. The mean vector length, r, can take values between 0 and 1 and serves as a measure of concentration as well as dispersion. The closer r is to unity, the less dispersed the directions are around the mean angle, Ø. The angle of deviation for the confidence interval, d, is used to determine the confidence limits ({ d), which in turn, are used to determine whether the sample mean angle, Ø, deviates significantly from the home direction azimuth before (07) or after (907) rotations. To determine the confidence limits in the present report, we chose the confidence coefficient, Q, to be 0.99. This coefficient is the probability that the unknown sample mean angle, Ø, will lie within the confidence interval. SPECIFIC METHODS AND RESULTS

The objective of the first experiment was to find out whether exploration is necessary for navigation with distal landmarks. Experiments II–VI were done to find out whether mice acquired during exploration information about the spatial relations between distal visual cues and the location of the nest entrance at the periphery of the arena. Experiment I The objective of this experiment is to find out whether exploration is necessary for navigation with learned distal landmarks. In other words, is prolonged straight line shuttling between two rewarded goals, without the benefit of any preceding exploration (undirected behavior for no obvious reinforcement), sufficient for learning the use of distal cues for homing?

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Two similar circular arenas were placed into two adjacent rooms that had a different layout and different distal cues. Naive mice were introduced into one of the arenas 1 day before the experimental trials. The experimental trials started by letting a mouse in one of the arenas retrieve its pups 40–100 times (depending on how avid the mice become in retrieving the pups) in order to strongly incite her retrieval motivation. Then the mouse was immediately removed from that arena and placed inside the nest of the other arena, with all of her pups placed right in front of the nest entrance. The mouse started immediately retrieving the pups, which kept being replaced in front of the nest hole until the mouse had retrieved about 20 times. After this the pups were replaced at gradually increasing distances away from the nest entrance until they were finally placed in the center of the arena. Some mice (25%) would ignore their pups and instead start exploring the novel environment. These exploring mice were removed from the experiment, and only strictly persistent retrievers were used further. This was necessary, since our objective was to test whether exploration, as defined in the introduction, was necessary for learning the distal cues or not. Using mice that have explored would defeat the purpose. After having retrieved pups 50–100 times from the center of the arena the mice were tested for distal landmark orientation: the arena was rotated 907 to the left or right while the mother was inside her peripheral nest. The mother would then leave the nest straight to the center on her own or was guided by the experimenter to this place by holding one of her pups in front of her. Finally, the direction of the returning (homing) path was determined at the moment the mouse arrived at periphery of the arena. Results All six mice that had been transferred to the unexplored novel environment returned close to the prerotation nest location (Ø Å 177, r Å 0.99, Fig. 1), rather than to the postrotation location at 907. The mice had a significant directional tendency (V test, v Å 5.56, p õ .0001). Hence, the hypothesis that free exploration is necessary for learning to navigate with distal cues has to be rejected. The bias of 177 toward the postrotation nest direction is significantly different from the 07 azimuth (99% confidence interval is 37 õ Ø õ 377). The plausible explanation for this bias is the superposition of relatively weak homing by path integration to the rotated nest location and strong directional homing by means of extra-arena cues to the prerotation nest location. Evidence for similar superimposition has previously been observed (Etienne et al., 1988; 1990; Alyan and Jander, 1994). Experiment II This experiment is to complement Experiment I: do mice acquire the use of distal cues for homing by exploring and without the benefit of straight line shuttling between two rewarded sites? Each of the seven mice used in this experiment was introduced into a

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FIG. 1. A schematic representation of the procedure used in Experiment I. (A) After a 24 hr exploration period, the mouse was induced to retrieve its pups from the center, back to the nest, for 40–100 times. The mouse was then carried and placed in a second arena located in a different, but adjacent room. (B) At the second arena, pups were already placed in front of the nest. The mouse started immediately retrieving them back to the nest of the new arena. (C) After 100 shuttles, the arena was rotated 907, while the mouse was inside the nest. The mouse then left the nest and headed to the center, picked up a pup, and took off toward the periphery. (D) The arrival points of six mice are shown. The arrow represents a mean vector, m, which is defined by its polar coordinates Ø and r. Ø is the sample mean direction and r is the length of m. The mean vector length, r, serves as a measure of concentration as well as dispersion. The larger r is, the less dispersed the directions are around the mean angle, Ø.

circular arena (only one circular arena was used in subsequent experiments) to allow her 1 full day of free exploration/investigation. The mouse had full access to the distal landmarks in the well-illuminated laboratory room. After this exploration period all pups were removed from the nest. The arena, with the mouse in its nest, was rotated 907, either clockwise or counterclockwise in order to control for intra-arena cues or proximal landmarks. Immediately thereafter the mouse was manually guided from the new rotated nest location through a convoluted path to the center of the arena (Fig. 2). This was achieved by continually luring the mouse with one of its pups held in front of it. The pup was suspended with its tail held between the soft (rubber) tips of forceps. The forceps kept the experimenter’s hand about 40 cm away from the pup, which was sufficient to prevent the mouse from fleeing and staying in its nest for fear caused by the proximity of the experimenter’s hand. While the pup was slowly moved horizontally the mouse closely tracked this movement. The convoluted path of this guided movement from the exit of the nest to the center of the arena comprised at least two U-turns and two full opposite rotations (Fig. 2). It lasted about 15 sec. At the end of the path, the pup was dropped and immediately picked up by the mother who then moved from the center to the periphery of the arena. The travel direction was recorded after the mouse had arrived at the periphery.

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FIG. 2. A schematic representation of the procedure used in Experiment II. (A) After a 24 hr exploration period, the arena was rotated while the mouse was inside the nest. (B) The mouse was guided in a convoluted path to the center of the arena, from where it took off towards the periphery. (C) Arrival points for the seven mice are shown.

The purpose of guiding the mouse through a convoluted path from the nest to the center of the arena was to weaken path integration, which is prone to rapid error accumulation as the length of the integrated path increases (Potegal 1987, Etienne et al., 1988, Matthews et al., 1988, Se´guinot, Maurer, & Etienne 1993). This weakening was expected to enhance the relative weight of alternative orientation strategies, if available. In order to achieve this objective we excluded from this experiment all mice that failed to continuously follow the convoluted guided path to the center of the arena. This happened when some mice abruptly stopped following the pup in front and went back to the nest and then immediately came out to follow the pup again. Results After 24 h exploration and weakened path integration, for the seven mice Ø was 57 (see Fig. 2), and r was 0.90. Thus, the mice had a significant directional tendency (V test, homeward component; v Å 6.29, p õ .0001). The mean angle falls within the confidence interval 3217 õ Ø õ 447. Therefore, Ø does not differ significantly from the azimuth of the prerotation nest location (07). This outcome decisively ruled out orientation by means of cues inside the arena and by means of path integration, because both mechanisms were expected to orient the mice toward the postrotation site of the nest at 907 . In addition, we reject the weaker hypothesis that mice tended to bisect directions of the pre- and postrotation nest locations by moving in the direction of 457. The only explanation left for this outcome is orientation by distal (extra-arena) landmarks. This indicates that the mice did form a representation of distal landmarks during the 24 h exploration period.

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Experiment III The objective of this and the following experiment is to quantify the relative strength of distal landmark orientation that has been acquired during 1 day of exploration. The idea is to establish an orientational conflict of 907 between finding home with distal landmarks and finding home by means of path integration. The mean direction taken by the homing mouse establishes the relative strength of these two orientation mechanisms. The amount of exploratory learning is kept constant in Experiment III and IV, but the strength of homing by path integration increases across the two experiments. In this experiment, the only opportunity for path integration for the mouse was given during one irregular search path. Each of 19 experimentally naive mice was introduced into a circular arena to allow her 1 full day of free exploration with full view of the distal landmarks in the well-illuminated laboratory room. After this exploration period all pups were removed from the nest. The arena, with the mouse in its nest, was rotated 907, either clockwise or counterclockwise. Two to three of the pups were scattered around the arena’ center, within a circle of 20 – 30 cm. The mother was allowed to leave the nest on her own. After leaving the nest, the mouse usually went in irregular self-generated search path. Curiously, some mice would tread on some of the pups while walking, oblivious of what they just did. Eventually, the mother would find one of the pups and retrieve it. This terminated the self-induced retrieval trial for that mouse. The direction taken by the mouse was taken to be the point of arrival at the peripheral fence. If a mother spent more than an arbitrarily decided period of 10 min outside the nest, without retrieving a pup, she was discarded. This was taken as a precaution to prevent the mice from forming a representation (although there is no evidence for such a quick process) based on distal cues in relation to the newly rotated nest location, which would confound the results. However, this may not have been enough precaution, and some may argue that the mice still formed a representation of distal landmarks, in whatever period they spent outside the nest, based on the new rotated nest position (again, there is no evidence for this), and thus homed by means of distal landmarks and not path integration. Therefore, a subset of 13 of the same 19 mice used above, were subjected to the procedure followed in Experiment II (guided by a pup in a convoluted path to the center of the arena), immediately following the self-induced retrieval trip, while the nest was still in its rotated position. Again, the point of arrival at the periphery was taken for directional analysis. If the mice arrived at the newly rotated nest location, this would indicate that the mice learned the distal cues based on the newly rotated nest location. However, if the mice arrived at the prerotation nest location, this would indicate that the mice representation of distal landmarks is still based on the prerotation nest location which was formed during the initial exploration period.

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FIG. 3. A schematic representation of the procedure used in Experiment III. (A) After a 24 hr exploration period, the arena was rotated while the mouse was inside the nest. (B) The mouse was left to find a pup on its own at the center of the arena, from where it took off toward the periphery. (C) Arrival points for the 19 mice are shown. (D) After retrieving one pup, the mouse was then guided by another in a convoluted path toward the center, from where it took off toward the periphery. (E) Arrival points for the 13 mice are shown.

Results After active search, for the 19 mice, Ø was 66.57 and r was 0.85 (Fig. 3). The mice had a significant directional tendency (V test, v Å 15.12, p õ .0001). The confidence limits are 44.57 õ Ø õ 88.57 (d Å 227, Q Å .99). Therefore, the mean angle of 66.57 does not differ significantly from the 457 azimuth. This indicates that homing was influenced by both path integration as well as distal cues as learned from the prerotation nest location. In contrast, after the guided search, for the subset of 13 mice, Ø Å 327 and r Å 0.84. The mice had a significant directional tendency (V test, v Å 5.87 in relation to 907, and v Å 9.2 in relation to 07, p õ .0001). This lies within the confidence limits 57 õ Ø õ 597. Thus Ø significantly differs from both the 07 and 907 azimuths, but not the 457 one. The mean direction taken by mice after active search was found to be significantly different from the mean direction taken after guided search at p Å .06 (Wilcoxon–Signed rank test, two-tailed). The mean direction of the group of mice after guided search is not significantly different from the mean direction of mice in Experiment II (Watson– William test, F Å 5.05, two-tailed, 0.1 õ p õ .25); Also, both groups did not differ significantly in their homing strength (angular dispersion; Mann– Whitney test, two-tailed, p Å .32). Therefore, after the 24 h exploratory experience and the self-induced search, mice homed by either path integration or by means of some intra-arena cue,

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FIG. 4. A schematic representation of the procedure used in Experiment IV. (A) After a 24 hr exploration period, the arena was rotated while the mouse was inside the nest. (B) The mouse was guided in a straight path to the center of the arena, from where it took off toward the periphery. (C) Arrival points for the six mice are shown.

an issue taken up in Experiment V. Guiding the mice through a convoluted path resulted in a homing direction that is a compromise between homing by path integration and distal landmarks, similar to what have been shown in Experiment II (see Etienne et al., 1990; Alyan & Jander 1994). Path integration in the course of one irregular search path only partially overrides the navigation by distal landmarks based on 1 day of exploration. Experiment IV The objective of Experiment IV is the same as in Experiment III, except that path integration is strengthened by allowing the mouse one guided straight line shuttle between the home and the distal target. For clarification, we used the same procedure under the same environmental conditions as in the Experiment II, except that after rotating the arena the mice were guided from the nest to the center of the arena on a straight rather than a convoluted path. Guidance, again, was implemented by continuously holding a pup in front of the walking mouse. Results In six such trials all six mice—after having been guided to the center of the arena—returned close to the postrotation nest location (Ø Å 77.57, r Å 0.98, Fig. 4). The mice had a directional tendency (V test, v Å 5.76, p õ .001). The 99% confidence interval is 577 õ Ø õ 937 ; i.e., is not significantly different from the expected direction of 907. A Mann–Whitney test for homing strength reveals that mice in Experiment II differ significantly in their homing

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FIG. 5. A schematic representation of the procedure used in Experiment V. (A) After a 24 hr exploration period, the arena was rotated while the mouse was inside the nest. (B) After turning the room lights off, and leaving only the arena lit, the mouse was guided in a convoluted path to the center of the arena, from where it took off toward the periphery. (C) Arrival points for the 13 mice are shown.

strength (homeward component) than mice in Experiment III (p õ .001). This comparison shows that after a convoluted outward path the mice prefer to home with the help of visual extra-area cues (Exp. II) whereas after a straight outward path they home largely on the basis of path integration (Exp. IV). Thus, orientation by path integration due to one straight line visit of a distal target is strong enough to override navigation by distal landmarks acquired during 1 day of exploration. Experiment V The outcome of Experiment II, homing by reference to extra-arena cues instead of intra-arena cues or by path integration, left open the sensory modality for detecting these extra-arena cues. To resolve this ambiguity, we prevented the homing mouse during the final testing procedure from using extraarena visual cues by turning off the room lights and illuminating only the inside of the arena. Otherwise, the procedure was exactly the same as in Experiment II. Mice were guided with one of the pups in a convoluted path to the center of the arena where the pup was then dropped for the mother to retrieve it. Results Under these conditions the average homing direction (Ø Å 857; r Å 0.88, Fig. 5) of the experimentally naive 13 mice tested is strikingly different from that in Experiment II. The strong hypothesis that the mean tendency of the

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mice is toward the postrotation nest location at 907 cannot be rejected (62.57 õ Ø õ 107.57). However, the weak hypothesis of tending to home halfway (457) between the pre- and postrotation nest location must be rejected. Based on past experience (Alyan and Jander, 1994), we account for this outcome by the assumption that the homing mice, after the removal of visual extraarena cues, guided their homing direction with information derived from integrating the convoluted outward path. However, we, again, cannot safely rule out the alternative hypothesis that the homing mice relied on some intraarena cues, such as odors. This ambiguity will be resolved in the following experiment (VI). Two of the 13 mice in this experiment moved in a direction closer to the prerotation than to the postrotation nest location (Fig. 5). This can be accounted for in two ways, between which we cannot decide. Either the two mice managed to access some extra-arena cues or, more parsimoniously, these two directions are only the extremes of a distribution centered around the post-rotation nest location. The angular deviation of the homing directions in this experiment (s Å {297) is larger than that in Experiment V (s Å {267). A Mann–Whitney test of dispersion (angular deviation) reveals that both groups are equally strongly homeward oriented (p Å 0.49). Therefore, we cannot claim that the directional accuracy of the dominating homing mechanism by means of distal landmarks was less accurate than that of the presumed orientation mechanism by path integration. Experiment VI Experiments II and III left open the question whether the mice, without recourse to extra-arena cues, homed by integrating their convoluted outward path or used some intra-arena cues. The objective of this experiment was to decide between these two alternatives. In Experiment VI, as in Experiments II and IV, the mice explored the arena 1 full day. Prior to testing we removed the view of distal landmarks by turning the room lights off and leaving only the arena lit. Then, as in the preceding experiments, we rotated the arena 907 with each mouse in the nest and we guided each mouse from the postrotation nest location through a convoluted path of at least two U-turns and two clockwise full rotations, to the center of the arena. While the mouse was in the center of the arena on a fixed platform, the arena was rotated back again so that the nest was located in the direction the mouse had experienced during exploration (07 in Fig. 6). Return orientation on the basis of path integration would take the mouse toward nest location after the first rotation (907 in Fig. 6) and return orientation by means of intra-arena cues to nest location after the second rotation (07). Results All six mice that were tested this way returned into the sector where the nest was located after the first rotation (Ø Å 697, r Å 0.97, Fig. 6). That is,

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FIG. 6. A schematic representation of the procedure used in Experiment VI. (A) After a 24 hr exploration period, the arena was rotated while the mouse was inside the nest. (B) After turning the room lights off, and leaving only the arena lit, the mouse was guided in a convoluted path to the center of the arena. (C) While the mouse was in the center, the arena was again rotated 907 to the original position. The mice took off toward the periphery. (D) Arrival points for the six mice are shown.

the mice had a directional tendency (V test, v Å 5.42, p õ .0001). The mean angle falls within the 99% confidence interval 447 õ p õ 947. Therefore, it is neither significantly different from the 907 or the 457 azimuths. This safely rules out control of the homeward direction on the basis of intra-arena cues with an expected direction of 07. It is plausible to attribute this deviation to a systematic error of path integration, because all mice were guided through two full clockwise rotations on their way to the center of the arena. DISCUSSION

Our experiments show for the first time that the house mouse does not have to engage in free exploration in order to learn to use distal landmarks for navigation purposes; they can also do this while shuttling between two goals (Experiment I and Experiment II). Exploration-based navigation by distal landmarks is provisional and so weak that path integration based on only one straight line excursion can override it (Experiment III). In striking contrast to this weakness, navigation by distal landmarks learned during repetitive straight line shuttling becomes so strong that it, in turn, overrides homing by path integration (compare Experiments I, II, and III). Given the great overall similarity (homology) in the topographic orientation mechanisms of all sighted rodents studied so far, there is a strong reason to

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believe that this dual mode of distal landmarks learning for navigation holds for all sighted rodents. The results of Experiment I demonstrated, for the house mouse, that, while exploration maybe sufficient, it is not necessary for the use of learned distal landmarks for short-range navigation. (Operationally, learning to navigate by means of distal landmarks is evident when a mouse, in a well-controlled context, takes a homeward direction that is clearly related to the position of the distal landmarks). Mere navigation between two goals without preceding exploration is an alternative mode of learning distal landmarks and then using them for navigation. If generalized, the theory of two distinct alternative modes of learning about distal landmarks adequately covers all known contexts in which any rodent has previously been found to learn about distal landmarks. These contexts, viz. learning during exploration (latent learning) and learning during navigation (incidental learning), have been reviewed in the introduction. Experiments II through VI demonstrated that exploration is sufficient for the mice to form a topographic representation of the experimental room during exploration (Experiment II). Following a convoluted path weakens navigation by path integration in favor of navigation by landmarks (Experiments II and III; also compare with Experiment IV), although when path integration is the only navigation mechanism available, homing by path integration can be as good as that by distal cues (Experiment V). Stepwise increasing strength of path integration from Experiment II to III to IV in the conflict between distal landmark orientation and path integration tells us that a single straight line excursion results in path integration that is just strong enough to override distal landmark orientation based on one day of exploration. Also, we found no evidence for a rapid formation of a representation of distal landmarks (over a period of 10 min or less; Experiment III). The nature of the distal cues used by mice to navigate are visual (Experiment V) and mice did not exhibit navigation by proximal or guiding intra-arena cues (Experiment VI). However, if exploration (again, defined as the whole collection of apparently undirected behaviors including movement through space, rearing, sniffing, location changes, etc.) is sufficient for learning the use of distal landmarks in navigation, it is puzzling that mice, having extensively explored, still emphasize path integration when commencing short-range shuttling between two goal points and that only after some experience with shuttling do they begin to use distal landmarks (Alyan & Jander, 1994). Clearly there must be some difference between exploration and shuttling in the way these two behaviors support landmark learning. The most parsimonious explanatory hypothesis for all presently known phenomena is merely a quantitative difference: we propose that the use of distal landmarks for navigation is learned by similar mechanisms during exploration and shuttling, but that the outcome from exploration is provisional or approximate and that during shuttling strengthening and fine-tuning of the landmark representation takes place.

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Learning the use of distal landmarks for navigation implies some representation in memory of the pertinent topographic layout, a representation commonly referred to as a cognitive map (Tolman, 1948; O’Keefe & Nadel, 1978; Wilson & McNaughton, 1993). Building a cognitive map has been made a defining characteristic of exploratory behavior (O’Keefe & Nadel, 1979; Thinus-Blanc et al., 1991; Toates, 1983; Tolman, 1948). Now we can add that such an exploration-based cognitive map can be further locally refined during nonexploratory shuttling between mapped goal sites. Exploration must have a second biological function besides the learning of distal orientation cues. How else could we explain the well-established fact that exploring rodents are so strongly attracted to proximal objects which they inspect at close range but later not use as cues to control navigation (Alyan & Jander 1994; also, see introduction)? We propose that the investigation of proximal objects during exploration has as its main biological function the learning of the spatial distribution of resources and dangers. In other words, exploration not only builds a map associated with orientation cues but also associates biological values with various mapped sites. This hypothesis is supported by various publications showing that after exploration rodents know what places to avoid, which way to escape from dangers, and where to find food or water when needed (Albert & Mah, 1972; Gleitman, 1955; Kendler, 1946; Renner, 1988; 1990; Seward, 1949; Sharp, Barnes, & McNaughton, 1987; Spence & Lippit, 1946). REFERENCES Albert, D. J., & Mah, C. J. (1972). An examination of conditional reinforcement using a onetrial learning procedure. Learning and Motivation, 3, 369–388. Alyan, S. H., & Jander, R. (1994). Short-range homing in the house mouse (Mus musculus): Stages in learning directions. Animal Behaviour, 48, 285–298. Archer, J., & Birke, L. V. A. (1983). Exploration in animals and humans. Wokingham, Berkshire: Van Nostrand–Reinhold. Barnett, S. A. (1958). Exploratory behaviour. British Journal of Psychology, 49, 289–310. Barnett, S. A., & Fraser, D. G. (1950). Pup-carrying by laboratory mice in an unfamiliar environment. Behavioral Biology, 14, 353–360. Barnett, S. A., & Smart, J. L. (1975). The movements of wild and domestic house mice in an artificial environment. Behavioral Biology, 15, 85–93. Batschelet, E. (1981). Circular statistics in biology. London: Academic Press. Berlyne, D. E. (1950). Novelty and curiosity as determinants of exploratory behaviour. British Journal of Psychology, 41, 68–80. Berry, R. J., & Bronson, F. H. (1992) Life history and bioeconomy of the house mouse. Biological Reviews, 67, 519–550. Best, P. J., & Thompson, L. T. (1989) Persistence, reticence, and opportunism of place-field activity in hippocampal neurons. Psychobiology, 17, 236–246. Blodgett, H. C. (1929). The effect of introduction of reward upon the maze performance of the rat. University of California Publications in Psychology, 4, 113–134. Boursot, P., Auffray, P.-J., Britton-Davidian, J., & Bonhomme, F. (1993). The evolution of house mice. Annual Reviews of Ecology and Systematics, 24, 119–152. Brown, L. E. (1966). Home range and movement of small mammals. Symposia of the Zoological Society of London, 18, 111–142.

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Poucet, B., Chapuis, N., Durup, M., & Thinus-Blanc, C. (1986). A study of exploratory behavior as an index of spatial knowledge in hamsters. Animal Learning and Behavior, 14, 93–100. Rabinovitch, M. S., & Rosvold, H. E. A. (1951). A closed-field intelligence test for rats. Canadian Journal of Psychology, 5, 122–128. Renner, M. J. (1988). Learning during exploration: The role of behavioral topography during exploration in determining subsequent adaptive behavior. International Journal of Comparative Psychology, 2, 43–48. Renner, M. J. (1990). Neglected aspects of exploratory and investigatory behavior. Psychobiology, 18, 16–22. Renner, M. J., & Rosenzweig, M. R. (1986). Object interactions in juvenile rats (Rattus norvegicus): Effects of different experiential histories. Journal of Comparative Psychology, 100, 229–236. Renner, M. J., & Seltzer, C. P. (1991). Molar characteristics of exploratory behavior and investigatory behavior in the rat (Rattus norvegicus). Journal of Comparative Psychology, 105, 326–339. Restle, F. (1957). Discrimination of cues in mazes : A resolution to the ‘‘Place-vs.-Response question. Psychological Review, 64, 217–228. Roullet, P., & Lasalle, J. M. (1990). Genetic variation, hippocampal mossy fibre distribution, novelty reactions and spatial representation in mice. Behavioural Brain Research, 41, 61– 69. Sales, S. M. (1968). Stimulus complexity as a determinant of approach behavior and inspection time in hooded rat. Canadian Journal of Psychology, 22, 11–17. Schenk, F. (1985). Development of place navigation in rats from waning to puberty. Behavioral and Neural Biology, 43, 69–85. Se´guinot, V., Maurer, R., & Etienne, A. S. (1993). Dead reckoning in a small mammal: the evaluation of distance. Journal of Comparative Physiology A, 173, 103–113. Seward, J. P. (1949). An experimental analysis of latent learning. Journal of Experimental Psychology, 39, 177–186. Sharp, P. E., Barnes, C. A., & McNaughton, B. L. (1987). Effects of aging on environmental modulation of hippocampal evoked response. Behavioral Neuroscience, 101, 170–178. Shillito, E. (1963). Exploratory behaviour in the short-tailed vole Microtus agrestis. Behaviour, 21, 145–154. Spence, K. W., & Lippit, R. (1946). An experimental test of the sign-Gestalt theory of trial-anderror learning. Journal of Experimental Psychology, 36, 491–502. Sutherland, R. J., & Dyck, R. H. (1984). Place navigation by rats in a swimming pool. Canadian Journal of Psychology, 38, 322–347. Suzuki, S. G., Augerinos, G., & Black, A. H. (1980). Stimulus control of spatial behavior on the eight arm maze in rats. Learning and Motivation, 11, 1–18. Thinus-Blanc, C., Chapuis, N., Bouzuba, L., Durup, M., & Poucet, B. (1987). A study in spatial parameters encoded during exploration in hamsters. Journal of Experimental Psychology: Animal Behavior Processes, 13, 418–427. Thinus-Blanc, C., Save, E., Buhot, M.-C., & Poucet, B. (1991). The hippocampus, exploratory activity, and spatial memory. In J. Paillard (Ed.), Brain and space (pp. 334–352). New York: Oxford Univ. Press. Toates, F. M. (1983). Exploration as a motivational and learning system. A cognitive incentive view. In J. Archer & L. V. A. Birke (Eds.), Exploration in animals and man (pp. 55–71). Wokingham, Bershire: Van Nostrand–Reinhold. Tolman, E. C. (1948). Cognitive maps in rats and man. Psychological Review, 55, 189–208. Tolman, E. C., & Honzik, C. H. (1930a). ‘‘Insight’’ in rats. University of California Publications in Psychology, 4, 215–232. Tolman, E. C., & Honzik, C. H. (1930b). Introduction and removal of reward and maze performance in rats. University of California Publications in Psychology, 4, 257–275.

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