The effect of a single light cue on homing behaviour of the golden hamster

Anita. Behav., 1990, 39, 17-41

The effect of a single light cue on homing behaviour of the golden hamster A R I A N E S. E T I E N N E , E V E L Y N E T E R O N I , C A T H E R I N E H U R N I & VERONIQUE PORTENIER Laboratoire d'~thologie, Facultb de Psychologie et des Sciences de l'Education, Universitb 2, CH-1211 Genbve 4, Switzerland

Abstract. Golden hamsters, Mesocricetus auratus W., tend to return directly from a food source at the centre of an experimental arena to their peripheral nest. The subjects' choice of a particular homing direction was tested in conditions where the animals could use simultaneously a weak light spot from outside the arena and self-generated signals derived from the outward journey to the food source. Conflicts between different categories of directional information were induced by shifting once or repeatedly the light cue from its standard angular position with respect to the nest entrance. While the subjects depended primarily on the light spot as a stable directional cue during minor conflicts, their homing behaviour became less homogeneous and was mainly controlled by self-generated signals when the conflict was increased. The light spot exerted its influence mainly during the phase of food collection, just before the subjects started to return to their nest; however, its impact remained noticeable even when it was presented only briefly at the beginning of the hoarding excursion, i.e. well before the initiation of the return trip. The choice of a final return vector may therefore imply stepwise information processing, whereby stored and actual values of visual information are compared with cues generated during the preceding outward journey.

In test conditions involving a rich optical background, maze learning in rodents depends primarily on visual cues from outside the maze (Munn 1950; Restle 1957; O'Keefe & Nadel 1978; Olton 1979; Suzuki et al. 1980; Pico & Davis 1984; Schenk 1985; O'Keefe & Speakman 1987). Little is known, however, about which components from the visual environment are selected as spatial criteria and how these components are organized to form a set of interrelated landmarks. One strategy for coping with this problem is to present the subjects with different 'visual worlds', ranging from a single visual cue to a plurality of configurations (Etienne et al. 1986a). Whatever the nature of these visual worlds, their role in controlling spatial orientation needs to be considered not only in terms of their own components and general structure, but also with respect to the subject's locomotor behaviour. As hypothesized by O'Keefe & Nadel (1978, page 94), to organize a visual environment, the subject has to relate changes in the perception of different cues to its own movements; at a later stage, the correlation between the preceding locomotor activity and the expected changes in its visual field may reinforce the recognition of a given location. Thus, spatial orientation implies the use of external 0003-3472/90/010017+25 $03.00/0

cues as well as an 'internal navigation' system, which keeps track of the subject's locomotor progression. Our own research on short-distance homing in the golden hamster, Mesocricetus auratus W., may well illustrate this intricate relationship between locomotion and the response to visual cues. During food hoarding, the hamster's return from a feeding place to its nest is controlled primarily by (1) stable optical configurations, which the animal perceives at the feeding place and has previously associated with the nest entrance; at the same time, however, it is influenced by (2) self-generated information, which is derived from the preceding outward journey to the food source. In other words, shortdistance homing by the golden hamster depends on actually perceived familiar cues as well as on the assessment of a preceding phase of locomotion by the above-mentioned internal navigation system. The extent to which the two categories of spatial information control the homing itinerary depends on the availability and nature of familiar cues from the visual background: the subjects orientate predominantly on the basis of visual information when tested under normal light, while in total darkness they depend entirely on self-generated

9 1990 The Association for the Study of Animal Behaviour 17

18

Animal Behaviour, 39, 1

information (Etienne et al. 1985; Teroni et al. 1987). The relative weight and mutual interaction of these two types of spatial information can be analysed thanks to the specific manner in which they govern the hamsters' homing behaviour. Under normal light, the animals orientate quite precisely with respect to the visual background. Thus, they maintain a constant homing direction in a constant visual environment. In darkness, in contrast, the subjects do not home in a constant direction with respect to their specific spatial environment. Rather, they return fairly directly to the point of departure of each particular hoarding trip; in other words, they orientate to the point in absolute space where they started to register the preceding outward journey to the food source. Further, the hamster's homing performance remains unaffected by a strong reduction of tactile, olfactory, auditory and geomagnetic cues, and occurs independently of specific features of the outward journey. It was therefore concluded that, without visual cues, the hamsters base their homing direction on self-generated cues; further, these 'internal' cues, which seem to consist mainly of proprioceptive and vestibular signals, are computed according to rules that yield a well-orientated homing vector (Etienne et al. 1985, 1986b). To analyse more closely the interaction between stable directional cues from the visual background and information depending on preceding locomotion, we started to test our subjects in visual conditions that involved only the presentation of a single, weak light spot (Teroni et al. 1987). Given that the hamsters started each hoarding excursion from a constant point of departure, namely the nest exit, they could learn to use this unique cue as an unambiguous directional reference. These experiments allowed us not only to investigate the interaction between the two above-mentionedcategories of spatial information, but also to distinguish between the relative roles of three classes of cues which the animal can theoretically use as directional criteria when tested in the presence of (one or several) visual configurations, namely: (i) the light spot as a stable and familiar directional reference from the environment, which is perceived 'in situ', i.e. at the point of departure of the homing trip; (2) the registration of the outward journey on the basis of purely internal self-generated signals; and (3) the light spot as a short-term reference for the registration of the outward journey. It

appeared that the animals' homing direction depended (1) primarily on the light spot as a familiar 'location-based' cue, (2) to a lesser extent on internal 'route-based' cues and (3) only to a very limited extent on the light spot as a 'route-based' cue, i.e. as an exteroceptive reference for assessing the outward journey. Attempts to distinguish unambiguously between location-based and routebased information (Baker 1984) can present difficulties (see below); however, we have kept this distinction because of its usefulness in highlighting the two alternative basic ways by which the subject can obtain spatial information, namely 'in situ' or 'en route'. These results were obtained in experiments that always involved the three above-mentioned categories of directional information, and that generally implied a conflict between two of these categories and the third one. In the first part of the present paper we describe a further attempt to define the influence of each particular type of information on the homing direction. Thus, the hamsters were presented either with only two categories of conflicting information, or with all three types, any two of which were in conflict with each other. The data from the first set of experiments confirmed that, within certain limits, the hamsters rely mainly on the light spot as a stable locationbased cue. Since a complete hoarding trip consists of a sequence of different phases, which follow each other in a strict spatial-temporal order (Etienne et al. 1983), it seemed worthwhile to examine when, during the hoarding excursion, the subjects derive directional information from the light spot. In a second set of experiments, the presentation of the light cue was therefore limited to a particular timespan, e.g. to the outward journey to the feeding place or to the uptake of food at the feeding place. Certain results of these experiments have implications as to the manner in which rodents combine different types of spatial information not only at the level of perception, but also at that of internal representation. GENERAL METHODS

Subjects Only adult females, which tend to be more consistently motivated to hoard than males (Etienne et al. 1983), were used. Several days before the beginning of the experiments each individual was introduced to its own arena, where it lived

Etienne et al.: Effect o f light cue on homing

/

Figure 1. Test apparatus. Each arena had a diameter of 220 cm and was surrounded by a peripheral wall 50 cm high. NB: nestbox. By pushing (and therefore lifting, see small curved arrow) a small circular door hinged at the top, the animal could enter the arena (see straight arrow) and reach the food source at the centre of the arena. The orientation of the return itineraries was coded by means of subdivisions on the floor of the arena which were reproduced on the video-monitor. Sawdust on the floor was stirred at regular intervals to erase olfactory and tactile cues. A video-camera, mounted above the centre of the arena, filmed each complete hoarding trip. A dim light spot (L) was mounted at the periphery of the arena, opposite to the nestbox, 13 cm above the upper border of the wall of the arena. During the experimental trials, the light spot was shifted from its standard position (see hatched arrows).

(alone) throughout the experimental period. The subjects were fed ad libitum and lived under a constant light cycle. Females that failed to establish their granary in the nestbox, or to hoard consistently or to show well-orientated control trials were excluded.

Apparatus Figure 1 shows the main features of the experimental set-up. In each experimental arena there was a single nestbox where the animal established its nest with a granary. This was fixed to the outside of the arena's peripheral wall. The door from the nestbox to the arena was always unlocked, so that the animals could move freely between the arena and their nest. To preserve a symmetrical pattern, the arenas had a number of additional permanently closed doors at regular intervals. The floor of the arena was subdivided by six diameters into 12 30~ and by six equidistant concentric circles into one circular (diameter 40 cm) and six annular zones. These subdivisions were reproduced on a transparent sheet covering the screen of a video-

19

monitor and thus enabled us to code the subject's displacements. The subject's itineraries were filmed under infrared light by a video camera. The light source consisted o f two diodes providing infrared light with a peak emission at 940 n m and a bandwidth of 45 nm. According to preliminary behavioural and electrophysiologicat data, golden hamsters do not respond to light with wavelengths o f 740 nm or more (Vauclair et al. 1977). The unique visual cue on which the animals could rely as a directional criterion was a dim light source, projected through a narrow slit to the centre of the arena, where it illuminated a small circular zone. To the fully adapted human eye no reflected light was visible beyond the central region of the arena. On the floor of the arena, the luminescence was of the order of 0.0046 cd/m 2 (centre), 0.001 cd/m 2 (30 cm from the centre) and 0-0001 cd/m 2 (periphery). Except in experiment IA, the light spot was introduced at least 2 days before the beginning of the experiments and was present throughout the dark phase o f the light cycle. Thus, the animals could establish a long-term association between the standard angular position of the light and the direction of the nest entrance.

General Procedures A typical hoarding excursion, during which the hamster collects food and carries it back to its granary, formed the basic unit of our experiments. The phases of the hoarding trip that occur outside the nest were monitored and systematically recorded throughout the experiments. (1) Outward journey: the animal left the nest exit and was led by means of a baited spoon as directly as possible towards a heap o f hazelnuts in the centre o f the arena. (2) Uptake of food ('hoarding'): at the food source, the animal took about 25-30 s to fill its cheekpouches; when doing this, each individual tended to turn to a lesser or greater extent around the heap of hazelnuts. (3) Return itinerary: the subject usually returned along a direct path to the periphery of the arena where it found the nest entrance either directly, or after exploratory movements along the arena's peripheral wall. The independent variables consisted of variations in the angular position o f the light spot with respect to the arena and in the timing of its presentation. The orientation o f the subjects' itinerary from the food source to the periphery of the arena repre-

20

Animal Behaviour, 39, 1

sented the main dependent variable. It was coded in terms of the 30~ in which the subject crossed successively the six concentric circles on the floor of the arena. As the animals sometimes tended to correct their homing direction while progressing from the food source to the periphery of the arena, special importance was given to the location of the subject when it crossed the last internal circle to enter the peripheral annular zone of the arena. As further parameters we recorded through which 30~ the animal entered or left the central zone containing the food source and the duration of its return from the centre of the arena to (1) its periphery and (2) the nest entrance. In the presentation of the results these parameters are mentioned only when they seem to play a decisive role in the orientation of the subjects. Subjects with a consistent motivation for hoarding were tested during a prolonged experimental period, during which they lived continuously in their arena. The experiments took place during daily testing sessions five times a week, in the evening, at the beginning of the dark phase of the artificial circadian cycle. One testing session included two or three test series, consisting of 8-12 hoarding excursions or trials. In each series, there was a systematic alternation between experimental and control trials. If an experiment included more than one independent variable, care was taken to permute in a systematic manner the different parameters. To eliminate tactile and olfactory trails or markings on the floor of the arena, the latter was covered with a thick layer of sawdust, which was thoroughly stirred and then flattened out again before each series of trials. For theoretical as well as empirical (Durup 1970) reasons it was assumed that the subjects' orientation could not be influenced by (stationary) olfactory cues from the nest or the peripheral wall of the arena as long as the animals had not entered the arena's peripheral annular zone. Acoustical cues were not masked in this research, as they do not seem to influence the orientation of the hamsters in our test conditions (Etienne et al. 1986b; E. Teroni, unpublished data). Throughout each experimental series, one experimenter, equipped with an infrared viewer, remained in the experimental room to lead the subject to the food source and to control the position of the light spot. The experimenter took care to change systematically her angular position with respect to the arena. The timing of the

presentation of the light spot was controlled by a second experimenter, who viewed the experiments from an adjacent room, on the video-monitor.

Statistics

As in former experiments, the subjects did not change their homing performance when tested repeatedly in the same experimental set-up, provided they had been introduced into the arenas and exposed to the light spot at least 2 days before the beginning of the experiments. This allowed us to treat the results of particular individuals during repeated testing in identical conditions by firstorder statistical tests (Batschelet 1981, personal communication). The Rayleigh test was used to examine whether a given subject yielded significant 'partial' vectors, i.e. was significantly orientated when it crossed each of the concentric circles on the arena floor during its repeated itineraries from the centre to the periphery of the arena. The method of confidence intervals allowed us to compare significant vectors pertaining to the subjects' orientation in a particular situation to the standard reference direction, which was defined by the radius vector pointing to the nest entrance. The same test was also used to evaluate the subjects' orientation with respect to other reference directions. The Wheeler-Watson test was used to compare significant vectors (r > 0.70) obtained from one subject in two different experimental situations' (for instance after a clockwise or counter-clockwise rotation of the light spot), or in one experimental situation and in the corresponding control conditions. In a second step, second-order statistics were applied to means of values obtained from particular individuals (Batschelet 1981). The mean vector for the orientation of the animals when they crossed the most peripheral circle on the arena floor (and thus entered the peripheral annular zone of the arena) was calculated for each experimental group. Moore's test was used to determine whether the distribution of the data was non-homogeneous. The distributions of the data from separate experimental groups were compared by the MardiaWatson-Wheeler uniform scores test. Our results are generally illustrated by first- and second-order statistics. (1) Depending on whether the data from particular subjects are homogeneous or not, the results from only one or several subjects are represented in a detailed manner, i.e. with

Etienne et al.: Effect o f light cue on homing respect to the mean orientation of the subjects when they crossed the six concentric circles on the floor of the arena. To summarize the results, the mean orientation of all subjects when they entered the peripheral annular zone of the arena is indicated on a single circle or quadrant. (2) The same circle or quadrant also contains the second-order vector which represents the orientation of the entire experimental group at the moment the animals entered the peripheral zone of the arena. Two temporal measurements of the homing performance were taken, namely the time the animals took to reach, from the arena centre, the most peripheral circle on the arena floor and the entrance of the nestbox. The temporal values obtained in the experimental trials were compared with those of the control trials by the Wilcoxon matched-pairs signed-ranks test (Siegel 1956).

21

ated information (Etienne 1987; Etienne et al. 1988). Thereafter, the light spot was presented from different directions. Under these conditions, the homing direction was expected to depend only on the light spot as a familiar location-based cue, which was no longer opposed by conflicting routebased information. In three further experiments the animals were presented with all three categories of spatial information, each of these categories being set in conflict with the two others. Thus, the animals were confronted with a three-fold contradiction between the light spot as a (1) familiar location-based or (2) temporary route-based cue and (3) the internal assessment of the outward journey. The three experiments ID 1, 2 and 3 presented three different combinations of conflicting information. Experiment IA: Two Classes of Route-based Information

EXPERIMENT h C O N F L I C T I N G CUES Two initial series of experiments provided the subjects with only two categories of conflicting directional information. Experiment IA created a conflict between the two kinds of route-based information the subjects could rely on, i.e. the registration of the outward journey with or without the (unfamiliar) light spot as an external reference system. In experiment IB the (familiar) light spot was presented after the end of the outward journey from an angle that differed from its usual position. This induced a conflict between the spot as a familiar directional cue and internal information derived from the outward journey. In our experimental set-up the subjects could easily be deprived of spatial information from the environment. Switching the light spot off (1) during or (2) after the outward journey to the food source meant that the animal (1) could no longer assess the outgoing trip with help of an external reference or (2) could not use a location-based directional cue at the moment it chose to begin the return trip. However, 'internal' route-based information, such as proprioceptive and vestibular cues, are automatically generated during the outward trip and therefore can never be withheld in an absolute manner. In experiment IC we attempted nevertheless to neutralize these cues. At the end of an outward journey occurring in complete darkness, the subjects were rotated to an extent expected to neutralize the previous registration of self-gener-

Methods The light spot was presented to the subjects only during the test situation. In all trials, the spot was positioned either opposite to, or behind the nest entrance during the outward journey. Care was taken to alternate regularly between these two positions to prevent the subjects forming a stable association between the angular position of the spot and that of the nest entrance. Throughout the control trials, the spot remained in the same position; in the experimental trials, its angular position was altered by 90 ~ (clockwise or counterclockwise) at the end of the outgoing trip, as soon as the subjects had started to collect food at the centre of the arena. Each subject (N= 4) underwent 32 control and 32 experimental trials. Results Figure 2 (small circles) indicates the expected homing directions the subjects would take if they had registered the outward journey with (Rv) or without (Ri) the light cue as an external reference. Without the light cue, they would return to their nest by reversing the resultant direction vector at the end of the outward journey. With the light cue, they would invert the relationship between the location of the light spot and the direction in which they had progressed during the outward journey. (If, for instance, the spot was positioned in front of a subject during its journey to the food source, the animal would move away from it during the return to the nest.) As the experimental trials implied a

Animal Behaviour, 39, 1

22

0

-I- 9 0 ~

-- 9 0 ~

(a)

(b)

Figure 2. Experiment IA. Conflict between the two classes of route-based information. During the outward journey, the light spot was presented either (a) opposite to or (b) behind the nest. The numbers on top of the figure indicate the angular amount by which the spot was rotated at the end of the outward journey (0~ control trials; 90~ experimental trials; +: clockwise rotation; - : counter-clockwise rotation). Circles indicate the theoretical homing directions if the subjects depended either on internal (Ri, continuous arrow) or on visual (Rv, dotted arrow) route-based information. NB: nestbox. The positions of the light spot during (O) and after (O) the outward journey are indicated. The curved arrows represent the angular shift of the light spot during the experimental trials. Quadrants show first- and secondorder data; they pertain to the subjects' orientation when the latter entered the peripheral zone of the arena in 16 control trials and in eight experimental trials of each category. In each quadrant the small black arrowheads represent the firstorder vectors (P < 0.01 and P < 0.05, Rayleigh test) of four subjects. The vectors with a large open arrow (double line: P < 0.01; single line: P < 0-05; Moore's test) represent the mean orientation of the entire experimental group. The length of the vectors is proportional to the radius of the quadrant, which is equal to one.

Etienne et al.: Effect o f light cue on homing 90~ of the spot at the end of the outward journey, the angular information yielded by the two types of route-based cues always differed by 90 ~. The first-order data of this experiment showed that all but one animal maintained consistently a significant orientation in both experimental situations (i.e. after a clockwise or a counter-clockwise rotation of the spot). Our four subjects tended to orientate towards the nest, but showed at the same time deviations from the 0~ direction (Fig. 2). Whereas non-significant deviations did not necessarily reflect the influence of the rotation of the light cue, this was the case for significant ( P < 0.05, method of confidence intervals) deviations from the 0~ direction. In this respect, our first-order results express a slight influence of the light spot as a route-based cue. Furthermore, three subjects took significantly longer to reach the nest entrance from the arena centre in the experimental than in the control trials (P<0.05, Wilcoxon matched-pairs signed-ranks test). The same tendencies appear on the level of second-order results (Fig. 2). Three of the four experimental vectors showed deviations that followed the direction in which the spot had been rotated but these are not significant. From a qualitative point of view, it must be mentioned that the presentation of the unfamiliar spot, with which the animals were confronted in the dark, strongly interfered with their motivation to hoard. Certain hamsters, intrigued by the new visual cue, either completely ceased to hoard and thus had to be excluded from the experiment, or did not immediately collect food upon their arrival at the food source and therefore had to undergo the same trials repeatedly. Experiment 113:Internal Route- and Location-based Information

Methods Throughout the experimental period, the spot was maintained in its standard position, opposite to the nestbox. Within the experimental sessions, the spot was turned off during the outward journey and presented only while the subjects collected food in the centre of the arena and during their return to the nest. In the control trials, the spot was in its standard position. In the experimental trials, the spot was presented at an angular distance of either (1) 90 ~ (clockwise or counter-clockwise) or

23

(2) 180 ~ with respect to its standard position. In test situation (1), each subject (N=12) underwent 20 control trials and 20 experimental trials, the spot being shifted alternately clockwise or counterclockwise; in test situation (2), the subjects ( N = 5) underwent 10 control and 10 experimental trials.

Results (1) 90~ between location-based and route-based information. In our experimental conditions, the standard position of the spot was facing the nest entrance. Should the subjects form a longterm, location-based association between the spot and the direction of the nest, they would return to the arena periphery in a direction opposite to the location of the light spot. Internal route-based information, on the other hand, always directs the subject back to the point of departure of the hoarding trip. The experimental trials, which involved a 90~ of the spot before its presentation at the end of the outward journey, confronted the hamsters with a 90~ between visual location-based (Lv) and internal route-based (Ri) directional cues (Fig. 3a). All the animals clearly responded to the light spot as a long-term cue. Moreover, nine out of our 12 subjects produced consistent sequences of experimental vectors deviating by more than 45 ~ from the nest entrance, and therefore reflecting primarily the effect of the light spot as a long-term cue (Fig. 3b, c). Thus, in both experimental situations, the partial vectors of eight of these animals differed consistently from the 0~ direction (P < 0.01, method of confidence intervals); at the same time, in general, these vectors did not differ significantly from the direction that points away from the light spot and therefore reflects the exclusive influence of the spot as a familiar visual cue (P~>0.05, method of confidence intervals). Throughout the two experimental situations, the nine above-mentioned subjects produced sequences of vectors that differed significantly from the corresponding control vectors; furthermore, all subjects orientated in different directions in the two experimental conditions (P < 0.05, Wheeler-Watson test). Finally, 10 of our 12 subjects took consistently longer to reach the nest entrance from the arena centre in the experimental than in the control trials (P<0-05, Wicoxon matched-pairs signed-ranks test); upon reaching the periphery of the arena at the wrong place, these subjects often

Animal Behaviour, 39, 1

24

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+90

~

--90 ~

(a)

9

Q

(b)

~ 1 7 6 ~176

(c)

Figure 3. Experiment IB 1.90~ between internal route-based information and the spot as a location-based cue. The numbers on top of the figure represent the deviation of the spot from its standard position during the control (0 ~ and the experimental ( + 90 ~ trials. (a) The theoretical homing directions if the subjects depended either on internal route-based information (Ri, continuous arrow), or on the light spot as a location-based cue (Lv, hatched arrow). NB: nestbox; e: the angular position of the light spot which appeared at the end of the outward journey. (b) The detailed orientation of one subject. The six vectors of equal magnitude ( P < 0.01, Rayleigh test) in each circle represent the subject's mean orientation when it crossed the six concentric circles on the floor of the arena; each point around the circles indicates in which 30~ the animal entered the arena's peripheral zone in 20 control trials and in 10 trials of each experimental situation. (c) First- and second-order data. In each quadrant, the small closed arrowheads represent the first-order vectors (P < 0.01 and P < 0.05, Rayleigh test) of 12 subjects when they entered the peripheral annular zone of the arena. The large open vectors (P<0.01, Moore's test) represent the mean orientation of the entire experimental group. The length of the vectors is proportional to the radius of the quadrant.

persisted in searching for the nest entrance in a direction opposite to t h a t o f the light spot. Second-order data fully confirmed these h o m o geneous results (Fig. 3c): The two experimental vectors p o i n t mainly away f r o m the light spot. They differ very significantly f r o m each o t h e r a n d f r o m the control vector ( P < 0 - 0 0 1 , M a r d i a - W a t s o n - W h e e l e r test).

(2) 180~

between location-based and

route-based information. To intensify the conflict between the light spot as a long-term visual cue a n d internal route-based i n f o r m a t i o n , the spot was rotated by 180 ~ before its presentation at the e n d o f the o u t w a r d journey. Thus, in the experimental trials, the spot a p p e a r e d just a b o v e the nestbox entrance. Now, the h a m s t e r s o u g h t to deviate by 180 ~ f r o m the nest if they based their directional choice o n the light as a location-based cue (Fig. 4a).

Etienne et al.: Effect o f light cue on homing

0o

180 ~

(a) 9

(b)

(c)

~

o

(d)

Figure 4. Experiment IB2. 180~

between internal route-based information and the spot as a locationbased cue. (a) The theoretical homing directions if the subjects depended either on internal route-based information (Ri) or on the light spot as a location-based (Lv) cue. (b) and (c) The detailed orientation of two subjects which underwent I0 control trials and 10 experimental trials. (d) The first-order and second-order vectors (double line: P < 0-01; single line: P < 0.05; Moore's test) from five subjects. For further explanation, see Fig. 3.

The familiar visual cue, however, influenced the animals' directional choice much less than in the preceding experiment. One subject returned precisely towards the nest (Fig. 4b), while the four remaining animals deviated by a mean angular amount ranging from 3 to 62 ~ from the nest entrance and showed an increased dispersion of

25

their homing directions (Fig. 4c, d). The majority of partial experimental vectors produced by these subjects differed significantly from the 0~ direction (P < 0.05, method of confidence intervals) or from the corresponding control vectors (P < 0-05, Wheeler Watson test). The second-order experimental vector (Fig. 4d) points mainly towards the nest. As it is based on somewhat heterogeneous results it is, however, significant only at the 5% level. Summing up, the two experiments which created a conflict between self-generated internal information and the light spot as a location-based cue yielded different results. During a 90~ the majority of animals depended in the first place on the light spot, and in the second place on selfgenerated information. The maximization of the conflict, however, inverted the order of priority of the two categories of directional cues. It also led to a greater dispersion of the homing directions within and between individuals.

Experiment IC: Neutralization Information

of Route-based

Methods Throughout the experimental period, the spot was maintained in its standard position, opposite to the nestbox. In all trials, the animal was led in complete darkness to a platform at the centre of the arena, where it found the food source. The experiment combined two categories of trials. During the uptake of food, the platform either remained stationary or was rotated by two full turns in one direction, followed by two full turns in the opposite direction, followed by a clockwise or counterclockwise rotation of 90 ~. In all trials, the light spot was turned on 16 s after the beginning o f food intake, i.e. the average timespan necessary to rotate the animals in the rotation-trials. The position of the spot was varied as in experiment IB1. In the control trials, the spot appeared in its standard location; in the experimental trials, it was presented from an angle that differed (clockwise or counterclockwise) by 90 ~ from its usual position. The subjects ( N = 4 ) underwent 10 trials of each category, and 60 trials in all. Results This experiment involved two variables. The light spot was presented as a familiar locationbased cue after the end of the outward journey and maintained in a constant position until the end of

26

Animal Behaviour, 39, 1

the hoarding excursion. In the control trials the light cue appeared in its usual position, whereas in the experimental trials the spot was moved 90 ~ from its standard location. A further variable consisted in the rotation of the animal at the arena centre, during the collection of food. It was expected that this procedure would reduce, or even abolish, the influence of route-based information which the animal had generated during the outward journey to the food source. Whenever the light spot had been rotated by 90 ~ (Fig. 5a), its influence (Lv) on homing behaviour was expected to deviate the animal by 90 ~, independently of the subject's own rotation. Self-generated information (Ri), in contrast, ought to lead the animal back to the nest entrance and was assumed to exert a stronger influence when hoarding occurred on a static than on a rotating platform. The first-order data from one animal well illustrates the homing behaviour shown by our four subjects (Fig. 5b, c). In all trials where the light spot had been rotated, the homing vectors differ significantly from the 0~ direction (P
trials where the light spot had been rotated than in the corresponding control trials; whereas this difference was significant in only 50% of the static experiments, it was always significant in the experiments that involved the rotation of the subject (P
Experiment D: Conflict Between the Three Types of Information

Methods Throughout the experimental period, the spot was maintained in its standard position, opposite the nestbox. In the control trials of the three experiments, the spot remained in its standard position throughout the trial. In the experimental trials, the light spot appeared in two different positions, the first (l) during the outward journey and the second (2) from the beginning of the uptake of food at the arena centre until the end of the return itinerary. Thus, in all experiments, each category of information was set either in a 180~ conflict or in a 90~ with the two other categories of information.

Experiment ID1. 180~ between internal and visual route-based information. The spot was (1) located 90 ~ (clockwise or counter-clockwise) with respect to its standard position, and then (2) rotated by 180~ (N= 4).

Experiment 11)2. 180~ between locationbased and route-based visual information. The spot was (1) located 180~ from its standard position (i.e. behind the nestbox) and then (2) rotated by 90 ~ (clockwise or counter-clockwise; N = 4).

Experiment ID3. 180~ between visual location-based and internal route-based information. The light spot was (1) positioned 90 ~ (clockwise or

Etienne et al.: Effect o f light cue on homing

0 o

+90

o

27

-90

~

(a)

9

+

s 0 C) ~176

~176

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Figure 5. Experiment IC. Effect of the light spot as a location-based cue after neutralizing internal route-based information. (a) The theoretical homing directions if the subjects depended either on internal route-based information (Ri) or on the light spot as a location-based cue (Lv). (b) and (c) The detailed orientation of one subject which collected food items either on a stationary (S) or on a rotating (R) platform. In each situation the subjects underwent 10 trials. (d) and (e) First- and second-order vectors from four subjects. For further explanation see Fig. 3.

Animal Behaviour, 39, 1

28

0o

180 o

180 ~

(a)

(b)

~

!iii!.

~

0

(c)

L? Figure 6. Experiment ID1. Conflict between the three categories of information, internal and visual route-based information being opposed by 180~ The numbers on top of the figure indicate the angular shift of the light spot at the end of the outward journey. (a) The theoretical homing directions if the subject depended on internal route-based information (Ri, continuous arrow), on the light spot as a route-based cue (Rv, dotted arrow) or on the light spot as a location-based cue (Lv, hatched arrow). The angular positions of the light spot during (o) and after (o) the outward journey are indicated. The curved arrows indicate the angular shift of the light spot during the experimental trials. (b) The detailed orientation of one subject in 20 control trials and in 10 trials of each experimental situation. (c) Firstand second-order vectors from four subjects. For further explanation, see Fig. 3.

counter-clockwise) with respect to its standard position, and t h e n (2) rotated (clockwise or counter-clockwise) by 90 ~ so that it was situated behind the nestbox ( N = 6). In all experiments, the animals underwent 20 control trials and 10 experimental trials of each type.

Results Experiment I1). The successive displacements of the light spot created a situation in which the light

spot as a route-based cue (Rv) indicated a homing direction opposite to that of the nestbox, while the spot as a location-based cue (Lv) indicated a direction which deviated by 90 ~ from the nest and therefore from the direction the subjects would derive from the (internal) registration of the outward journey (Ri) (Fig. 6a). These conditions yielded homogeneous results, which are illustrated by the first-order data in Fig. 6b, c. In both experimental conditions, the subjects orientated in a direction that seems to

Etienne et al.: Effect o f light cue on homing represent a compromise between internal routebased information and the light spot as a familiar, location-based cue. Throughout the experiment, three of our four subjects yielded consistent sequences of very significant (partial) vectors, which differed from the 0~ direction (P < 0"01, method of confidence intervals), but also from the direction suggested by the light spot as a location-based cue (P < 0-05, method of confidence intervals). Further, these subjects differed consistently in their directional choices if one compares the control trials with the corresponding experimental trials, and the two sets of experimental trials with each other (P < 0.05, Wheeler-Watson test). Finally, during their return only one subject took more time to reach the peripheral annular zone in the experimental than in the control trials (P<0.05, Wilcoxon matched-pairs signed-ranks test), whereas all four subjects took more time to reach the nest entrance during the experimental trials (P<0.01, Wilcoxon matched-pairs signedranks test). The deviation from the 0~ direction of the second-order vectors (Fig. 6c) is close to 45 ~ and thus seems to express the animals' preference for a compromise direction between internal routebased information and the spot as a location-based cue. At first sight the light spot as an external reference for the registration of the outward journey does not seem to have influenced the animals' homing behaviour. However, comparison between these data and the results of experiment IB1 suggests that the presentation of the light spot during the outward journey may well have played some role, as will be discussed more explicitly below. Experiment ID2. This experiment again involved a 90~ between internal route-based information (Ri) and the light spot as a location-based cue (Lv), whereas route-based (Rv) and locationbased (Lv) visual information differed by 180~ (Fig. 7a). Second-order data (Fig. 7c) again indicate a compromise between the effect of the light spot as a location-based cue and self-generated route-based information, with a slight predominance of the influence of the light spot as a familiar cue. At first glance, route-based visual information seems to play hardly any role. Our first-order data (Fig. 7b, c) however, yield a less homogeneous picture than in the preceding experiment. The partial experimental vectors from particular individuals are

29

always significant, yet can be classified into three different categories. (1) The vectors reflect the above-mentioned compromise; (2) they come nearer to the radius vector pointing 90 ~ away from the nest than in category (1); and (3) they point, very exceptionally, more towards the nest than in category (1). Thus, the weights of internal routebased and location-based information differed between or even within individuals if one compares the responses of certain subjects in the two experimental situations. For all subjects, the sequences of partial vectors differed from each other in the two experimental situations (P < 0-01, Wheeler-Watson test). Further, the majority of partial vectors differed significantly from the 0~ direction (P < 0-01, method of confidence intervals), whereas they differed less regularly from the radius vector pointing 90 ~ away from the nest. On the whole, our subjects showed a less homogeneous directional choice in this experiment than in the conditions of experiment ID1. Interestingly, three of the four subjects took significantly more time to reach from the food source, not only the nest entrance but also the peripheral annular zone during the experimental than during the control trials (P<0"05, Wilcoxon matched-pair signedranks test). This tendency can be interpreted as a sign of hesitation in the choice of a given direction. Again, the comparison between these results and those of experiment IB1 indicates that the presentation of the spot during the outward journey may have exerted some effect on the subjects' behaviour. Experiment ID3. In contrast to the two former test situations, experiment ID3 created a 180~ conflict between the light spot as a location-based cue (Lv) and internal route-based information (Ri), and 90~ between the two preceding categories of directional information and the light spot as a visual reference for the registration of the outward journey (Rv; Fig. 8a). These conditions induced very heterogeneous results (Fig. 8e). Only two subjects remained significantly orientated throughout their homing itineraries and returned mainly towards the nest (Fig. 8b). The four other subjects yielded in either one or both experimental situations partial vectors that did not reach the level of significance (Fig. 8c, d). Some of these vectors suggest the intervention of different cues or a combination of cues, among which the light spot as a route-based reference seems to play a relatively greater role than

Animal Behaviour, 39, 1

30

-t-90 ~

0o

-90

~

(a)

(b)

,,

(c)

ly

, ,

Figure 7. Experiment ID2. Conflict between the three categories of information, location-based and route-based visual information being opposed by 180~ (a) The theoretical homing directions if the subjects depended on internal routebased information (Ri), on the light spot as a route-based cue (Rv) or on the light spot as a location-based cue (Lv). (b) The detailed orientation of one subject. (c) First-order and second-order vectors (double line: P < 0.01; single line: P < 0.05, Moore's test) from four subjects. For further explanation, see Fig. 6.

in o u r f o r m e r experimental situations. In further c o n t r a s t to o u r other results, we observed discontinuities in the a l i g n m e n t of partial vectors (Fig. 8c, d). This tendency m a y be due to the fact t h a t the subjects shifted from one reference to a n o t h e r while they progressed from the centre to the periphery of the arena. All o f these four subjects took significantly longer to reach the nestbox e n t r a n c e from the a r e n a centre in the experimental trials t h a n in the control trials ( P < 0"01; Wilcoxon

matched-pairs signed-ranks test). The lack of h o m o g e n e i t y of o u r results led to non-significant second-order vectors (Fig. 8e). Summarizing, these results show t h a t when there is a general conflict between o u r three categories o f directional information, internal route-based cues gain in i m p o r t a n c e a n d the h a m s t e r s resort mainly to a c o m p r o m i s e between these cues a n d the light spot as a location-based cue. The state o f conflict is e n h a n c e d in experiment ID3, which involved in

Etienne et al.: Effect o f light cue on homing

0~

+90*

-90

31

~

(a)

(b)

@.,,,,,.@,, @.,:

(c)

(d)

Figure 8. Experiment ID3. Conflict between the three categories of information, visual location-based and internal route-based information being opposed by 180 ~ (a) The theoretical homing directions if the subjects depended on internal route-based information (Ri), on the light spot as a route-based cue (Rv) or on the light spot as a location-based cue (Lv). (b), (c) and (d) The detailed orientation o f three subjects in 20 control trials and in 10 experimental trials of each category (solid vectors: P < 0.01: hatched vectors: P < 0.05; dotted vectors: P/> 0-05; Rayleigh test). (e) First- and second-order data from six subjects. The arrowheads represent the mean orientation (closed head: P<0.01 and P < 0.05; open head: P i> 0.05; Rayleigh test) of each particular subject when it entered the peripheral zone of the arena. The large open arrowheads represent the second-order vectors (double line: P < 0.01; dotted line: P t> 0.05; Moore's test) of the entire experimental group. For further explanation, see Fig. 6.

addition a 180~ between location-based a n d i n t e r n a l r o u t e - b a s e d i n f o r m a t i o n . I n this situation, either t h e subjects a t t r i b u t e still m o r e i m p o r t a n c e to self-generated i n f o r m a t i o n , o r they are n o l o n g e r significantly o r i e n t a t e d .

EXPERIMENT INFORMATION

II" T I M I N G O F COLLECTION

T h e precise spatial a n d t e m p o r a l o r g a n i z a t i o n o f h o a r d i n g b y the g o l d e n h a m s t e r s e e m e d to offer

32

Animal Behaviour, 39, 1

ideal conditions for examining when, in the course of one particular hoarding trip, the subject registers different categories of spatial information. By definition, route-based information that controis the return itinerary from a food source to the nest is registered during the outward journey of each particular hoarding trip. Reliance on internal route-based information requires, additionally, the continued registration and computation of any change in orientation occurring at the food source. As the subject does not use an external reference to determine and store the resultant angular components of its outgoing itinerary, any locomotor activity occurring before the onset of the return must be taken into account to determine the final direction of the homing itinerary. If, in contrast, the registration of the outward journey has occurred with the help of an external reference, its final outcome at the end of the outward journey can be memorized with respect to this reference and retrieved just before the return, provided the reference is still available. Should the latter disappear after the performance of the outward journey, then the subject could still benefit from this registration of the outgoing trip (i.e. the precision of this registration may be enhanced through the use of the external reference). However, after the elimination of the visual cue the animal must be capable of switching to a purely internal mode of integrating all further changes occurring in its own orientation before the beginning of the return itinerary. On the other hand, location-based information might be collected on site, before departure (i.e. before the start of the return itinerary), and this information might be independent of the immediately preceding phase of locomotion. Once the subject has started its itinerary on the basis of location-based cues, it may adjust its locomotion to the same cues or to further location-based landmarks encountered at new sites. In our experimental situation, the hamsters usually return fairly directly, in less than 3 s, from the centre to the peripheral annular zone of the arena. The subjects should therefore choose a particular homing direction at the arena centre, before leaving the latter, and should then return to the arena periphery without further reference to location-based cues. The following experiments were carried out to determine the impact of the light spot on the animals' homing direction when its presentation is limited to specific phases of the hoarding excursion.

In experiment IIA 1, the spot was presented during the outward journey, until the animals had clearly started to collect food items at the arena centre9 In these conditions, the spot exerted an unexpected, significant location-based effect on the homing behaviour (see below)9 Two further experiments IIA2 and IIB were therefore carried out to determine whether the subjects had gained directional information from the light spot only at the arena centre, or also during the outgoing trip. The impact of the presentation of the light cue after the end of the outward journey has already been described in connection with two former experiments. In experiment IB, the spot was presented from the beginning of hoarding to the end of the complete hoarding trip, and in experiment IC it was switched on 16 s after the initiation of hoarding and was kept on until the end of the return itinerary, as in the previous case. In a further experiment, IIC, we compared the subjects' orientation in two situations. The spot was presented either only during the hoarding phase, or during both the hoarding phase and the return to the nest. This procedure was intended to test our hypothesis that in our test conditions the return occurs under the control of a predetermined 'Sollwert', and is not corrected by any further reliance on the spot as a location-based cue.

General Procedures In all experiments, the light spot was introduced at least 2 days before the beginning of the test series. In the control trials, the spot was maintained in its standard location, opposite the nestbox. In the experimental trials, it was presented at an angular distance of 90 ~ (clockwise or counterclockwise) from its standard position. In each experiment, the spot appeared during a specific phase of the hoarding behaviour. Experiment HA: Presentation of Spot During Outward Journey Methods In the main experiment IIA1, the spot was presented from the moment the animal had left the nest and until the beginning of the food uptake, i.e. when hoarding had clearly been initiated. The animals (N=9) underwent 20 control trials and 10 experimental trials of each category. A control experiment IIA2 was carried out to see whether the extension of the presentation of the

Etienne et al.: Effect o f light cue on homing

0~

Ca)

+90 ~

oNB

33

-90 ~

9

9

(b)

(c)

Figure 9. Experiment IIA 1. Presentation of spot during outward journey and initiation of hoarding. The numbers on top of the figure indicate the deviation of the light spot from its standard angular position. (a) The theoretical homing directions if the subjects depended on internal route-based information (Ri), on the light spot as a route-based cue (Rv) or on the light spot as a location-based cue (Lv). The position of the light spot (o) is indicated. (b) The detailed orientation of one subject in 20 control and 10 experimental trials of each category. (c) First-order vectors (closed arrowhead: P<0.01 and P<0.05; open arrowhead: P~>0.05; Rayleigh test) and second-order vectors from nine subjects. For further explanation, see Fig. 3.

spot into the hoarding phase strengthened its influence. In 50% of the trials (1) the presentation of the light spot was limited to the strict performance of the outward journey, i.e. the spot was switched offas soon as the animals had reached the food source at the arena centre; in the remaining trials (2), the spot was switched off 5 s after the animals had arrived at the food source and started to fill their cheek pouches. The animals ( N = 6) underwent 30 trials (1) and 30 trials (2), the light spot being presented alternately in its standard position or with a 90~ from this position.

Results As mentioned beforehand, it was expected that in experiment IIA1 the animals would rely on the spot as a route-based reference. In this case, they ought to return directly to the nest, since there is no conflict between the registration of the outward journey with (Rv) or without (Ri) the spot as an external reference (Fig. 9a). However, to understand the outcome of this experiment, it is important to remember that the subjects had been exposed to the spot at its standard location before the testing period and therefore had formed a

34

Animal Behaviour, 39, 1

0o

+90 ~

Ca)

--90 ~

|

|

(b)

Figure 10. Experiment IIB, Presentation of spot at the beginning of the hoarding phase. (a) The theoretical homing directions if the subjects depended on internal route-based information (Ri) or on the light spot as a location-based cue (Lv). The small circles with a dot in the centre indicate the position of the light spot. (b) First- and second-order data from four subjects. The vectors pertain to 20 control trials and to 10 trials of each experimental situation. For further explanation, see Fig. 3.

stable association between the standard position of the spot and the direction of the nest entrance. Thus, the subjects could confuse the angle of presentation of the spot with its standard angular position, In this case, they would rely entirely on the spot as a familiar location-based reference (Lv). After the disappearance of the spot, the subjects may register their further movements around the food source on a proprioceptive and vestibular basis, but with the angular position of the familiar visual reference as a reference for initiating this registration. If this is so, one would expect them to return to the nest in a direction opposite to the angle of incidence of the spot during its initial presentation. The first-order data from this experiment (Fig. 9b, c) indicate quite distinctly that the light spot influenced the subjects' orientation in its quality as a familiar, location-based cue. In both experimental situations, all subjects but one ( N = 9) showed at least a slight deviation from the 0 ~ reference direction. This deviation always occurred

in a direction opposite to that of the presentation of the spot during the outward journey. F o r three subjects, the deviation from the nest entrance was consistently significant at the 1% level; for a further four subjects, it appeared at the 5% level in at least one experimental situation (method of confidence intervals). Eight subjects orientated either in one or in both categories of experimental trials differently from in the corresponding control trials; furthermore, these animals orientated differently in the two experimental situations ( P < 0 ' 0 5 , WheelerWatson test). Finally, four subjects took longer to reach the nest entrance in either one or both types of experimental trials than in the corresponding control trials (P<0"05, Wilcoxon matched-pairs signed-ranks test). These results from particular subjects are fully confirmed by second-order data (Fig. 9c). The experimental vectors express the predominant influence of internal route-based information, but they also show a clear deviation from the 0 ~ reference direction, attributable to location-based

Etienne et al.: Effect o f light cue on homing

visual information. Thus, the two experimental vectors differ significantly from each other (P<0.01) as well as from the control vector (P < 0-05; Mardia-Watson-Wheeler test). In experiment IIA1 we made sure that the subjects had clearly started to hoard food at the arena centre before switching the light spot off. Control experiment IIA2 was carried out to see whether the location-based influence of the spot depended on the extension of the time of presentation of the spot into the hoarding phase. The homing performance observed in the two conditions of this experiment can be summarized as follows. If the spot was switched out at the moment the animal reached the arena centre, it continued to exert a location-based effect on the subjects' homing behaviour; however, its influence was strongly reduced. In the experimental trials, three of our six subjects exhibited a consistent location-based deviation from the homing direction, but the deviation was never significant (P>~0"05, test of confidence intervals). Only one of these subjects orientated significantly differently in the two categories of experimental trials, i.e. after a clockwise or counter-clockwise rotation of the spot (P < 0-05, Wheeler-Watson test). After the presentation of the spot during the outward journey and at the beginning of hoarding, the subjects showed, on average, an enhanced location-based deviation from the reference direction. In the experimental trials, four of our six subjects showed the expected deviations from the homing direction, two subjects having deviated significantly from the 0~ direction in both experimental situations (P < 0.05, method of confidence intervals). These two subjects showed significant differences in their control and experimental trials (P<0-05, Wheeler-Watson test). Finally, three subjects showed statistical differences in their orientation in both experimental situations (P < 0-05, Wheeler-Watson test). The statistical comparison between the homing behaviour observed in the experimental trials after different durations of presentation of the spot yielded no significant differences either on the level of first-order statistics (P~> 0.05, Wheeler-Watson test) or on that of second-order statistics (P~> 0.05, Mardia-Watson-Wheeler test). In summary, these results show that the spot exerted a slight location-based influence even when its presentation was strictly limited to the outward journey, and that its effect was enhanced (albeit not

35

significantly) by its additional presentation during the beginning of hoarding. In general, the six subjects of this experiment seemed less influenced by the spot than those tested in experiment IIA1.

Experiment liB: Presentation of Spot at Beginning of Hoarding Methods The spot was presented for 5 s, at the beginning of the food uptake at the arena centre. The animals ( N = 4 ) underwent 20 control trials and 10 experimental trials of each category. Results This experiment represents a further attempt to verify the results of experiment IIA1. Now, the spot was presented only during the initial 5 s of food uptake. For two of our four subjects, the presentation of the light spot at the beginning of hoarding consistently exerted a slight location-based influence (Fig. 10b). The vectors of these subjects in the two experimental situations differed from each other (P < 0"05), but not from the control vector (P ~>0.05, Wheeler-Watson test). These results led to second-order experimental vectors that deviated slightly from the 0~ direction, but did not differ significantly from each other (P >~0.10, Mardia-Watson-Wheeler test). Taken together, the data from experiments IIA and IIB suggest the following conclusions. Even when its presentation is strictly limited to the outward journey, the spot may exert a locationbased influence. This influence is enhanced if the spot is shown not only during the outward journey, but also during the beginning of hoarding. However, the presentation of the spot during the initial 5 s of hoarding influences only slightly the subjects' homing direction. It appears therefore that (1) the subjects always tend to rely on the spot as a familiar directional cue when it is presented at the beginning of the hoarding excursion, and that (2) the spot increases its location-based effect in proportion to the duration of its presentation. Most likely, point (2) is mainly linked to attentional factors. The subject is given much more opportunity to see the (weak) spot when the latter is presented in a continuous manner during the complete outward journey and at the beginning of hoarding than when the spot is presented only during the outward journey or only at the beginning of hoarding.

Animal Behaviour, 39, 1

36

0 o

(a)

+90

~

-90

~

.@

NB

(b)

g I

(c)

+ I

Figure l l. Experiment IIC. Presentation of spot during the hoarding phase, with or without its additional presentation during the return itinerary. (a) The theoretical homing directions if the subjects depended on internal route-based information (Ri) or on the light spot as a location-based cue (Lv). (b) and (c) First- and second-order data from five subjects. The test conditions involved the presentation of the light spot either during the hoarding phase (hoard) only, or during the hoarding phase and the return itinerary (hoard+return). In each of these conditions, the subjects underwent 10 control trials and 10 experimental trials of each category. For further explanation, see Fig. 3. Experiment IIC: Presentation of Spot During Hoarding and Return Methods In 50% of the trials (1) the light spot was presented only while the animal was collecting food at the arena centre; in the remaining trials (2) it was presented from the beginning of hoarding until the end of the trials. F o r further explanation, see experiment IIA2. Five animals were used. Results Let us now consider how the subjects react to the

light spot when it is presented after the end of the outward journey. Yielding the 90~ situation between the spot as a location-based cue and internal route-based information, experiment IB1 has already shown that the presentation of the spot from the beginning of hoarding to the end of the return itinerary exerts a strong effect on homing. According to the data of experiment IC, this effect is not reduced if the spot appears only during the second half of the hoarding phase. Experiment IIC was carried out to verify the hypothesis that the subjects do not adjust their

Etienne et al.: Effect o f light cue on homing homing itinerary to directional information provided by the light spot once they have initiated their return to the arena periphery. Thus, the same subjects were presented with the spot either during the hoarding phase alone (1), or during hoarding and the return to the nest (2). Our hypothesis is clearly supported by our results (Fig. 11). The second-order experimental vectors obtained in conditions (1) and (2) after a clockwise or counterclockwise rotation of the spot do not differ from each other. On the other hand, within identical conditions with respect to the duration of presentation of the spot, these vectors differ significantly from each other and from the control vector (P < 0'05, Mardia-Watson-Wheeler test). These second-order results are based on very clear-cut first-order data. The duration of presentation of the spot had no effect on the experimental vectors for single subjects. However, within conditions (1) and (2) the animals deviated in all experimental trials from the 0~ direction (P < 0.01, method of confidence intervals) and orientated differently if we compare the control and corresponding experimental trials, or the two categories of experimental trials involving a clockwise or counter-clockwise rotation of the spot (P<0-05, Wheeler-Watson test). Our data from this experiment also confirm the location-based effect of the light spot on the subjects' return time from the centre of the arena to the nest entrance. Four of our five subjects took consistently longer to return to the nest in the trials that involved a rotation of the light spot than in the corresponding control trials. On the other hand, the subjects took about the same time to return to their nest if we compare their homing behaviour in the experimental trials of the two situations (1) and (2), which differed with respect to the duration of the presentation of the spot. Thus, the spot influenced the subjects in their orientation from the centre to the periphery of the arena, but did not seem to interfere with their search of the nest entrance once they had reached the arena periphery.

DISCUSSION The data from both sections of this paper confirm our previous results with regard to the relative influence of our three categories of spatial information on short-distance homing in golden hamsters.

37

(1) A single light spot, presented during a certain timespan in a constant angular position with respect to the nest entrance, plays a major role as a familiar, location-based directional cue. (2) Internal route-based information derived from the preceding outward journey to the food source interacts with the light spot as a location-based cue throughout our experimental situations. The greater the conflict between the different types of spatial information the animals are presented with, the more the weight of self-generated cues increases compared with that of the familiar light spot. (3) Lastly, the hamsters seem to rely only a little on the light spot as a temporary reference for assessing the outward journey to the feeding place. In conditions of conflicting information (experiment I), the location-based influence of the spot appeared most clearly in experiment IB1 and throughout experiment IC (Figs 3 and 5). Whereas these experiments included no visual information during the outward journey, they implied a 90 ~ conflict between location-based and self-generated route-based information, i.e. the two categories of information the animals rely on most. In experiment IB2, where the conflict between these two types of information was raised from 90 to 180~ the subjects gave less homogeneous results and tended to rely more on the internal assessment of the outward journey (Fig. 4). One possible explanation for this result is that at the end of the outward journey the animal expects to see the light spot within a particular region. If the light cue is too far outside this region, the animal tends to ignore it. Highly contradictory situations, which involved a three-fold conflict between our three categories of spatial information, led either to a compromise between the influence of the light spot as a locationbased cue and self-generated information (experiments ID1 and ID2, Figs 6 and 7), or to a state of confusion, with the occasional prevalence of internal route-based information (experiment ID3, Fig. 8). These results show again that the relative weight of the familiar visual cue decreases in proportion to the state of conflict the subjects are exposed to. Experiments ID1 and ID2 implied a 90~ between the spot as a location-based reference and self-generated information, whereas these two classes of information indicated completely opposed homing directions in experiment ID3. The fact that hamsters are only slightly inclined to rely on the light spot as an external reference for assessing the outward journey appears most clearly

38

Animal Behaviour, 39, 1

in experiment IA (Fig. 2). The unexpected appearance of the visual cue seemed to confuse the subjects and exerted only a slight and inconsistent effect on their return itineraries. In conditions of a general conflict between our three categories of spatial information, on the other hand, the above-mentioned change in the relative weights of location-based and self-generated route-based information may well have been caused by the presentation of the light spot during the outward journey. Experiments ID1 and ID2 contained the same degree ofconffict between location-based and self-generated information as experiment IB1, but involved the additional presentation of the spot during the outward journey and its rotation at the beginning of hoarding. While the hamsters relied mainly on location-based information in experiment IB1, they resorted to a compromise between location-based and self-generated information in experiments ID 1 and ID2. That the presentation of the spot during the outward journey may occasionally influence in a more direct manner the assessment of route-based information is suggested by the (heterogeneous) results of experiment ID3 (see above). From a functional point of view, these results suggest the following interpretation. As developed in more detail elsewhere (Etienne 1987; Etienne et al. 1988), stable configurations from the outside world allow a subject to organize its environment on a long-term basis. Route-based information, on the contrary, is stored in short-term memory and remains, by definition, available only within a given sequence of locomotor behaviour; furthermore, errors that occur in the stepwise assessment of route-based information have cumulative consequences and therefore impose short-range limitations on the use of path-dependent information. Thus, familiar location-based information is bound to exert a predominant control on a subject that has the capacity to choose and store specific features from the spatial environment as landmarks and to integrate the latter into an interrelated topographic system. In our test situation, the hamsters' visual environment was reduced to a strict minimum, i.e. a single, weak light spot presented in complete darkness. Because of the constant angular relationship between the standard position of the light spot and .that of the nest entrance, where the subjects always started their hoarding excursion, the animals could use the light spot as an unambiguous

location-based directional reference. However, a repeated shift of the spot and its 180~ to internal route-based information seemed to induce limits beyond which the light cue lost its reliability as a stable reference from the outside world. One may wonder why in our test conditions golden hamsters prefer to assess the angular component of the outward journey to the food place without the help of a temporary visual reference. To register and compute path-dependent information with respect to an external reference has obvious advantages. (1) At any moment of its locomotor activity, the animal can recheck the orientation of its X-axis with respect to the external reference and therefore control the accuracy with which it assesses the actual direction of its progression. (2) At the end of the outward journey, its resultant angular component can be memorized with respect to the external reference; this allows the animal to introduce a delay between the end of the outward journey and the beginning of the return itinerary without keeping track of its further angular displacements at the food source. The assessment of route-based information on the basis of internal signals, in contrast (1) cannot be controlled via a feedback loop, and (2) implies the continued registration of self-generated signals from the beginning of the outward journey to the beginning of the return itinerary. These differences impose much heavier limitations on the use of internal route-based information than on the assessment of the outward journey through the intermediary of an external reference. Our experimental procedures do not allow us to claim that hamsters do not use an external reference system for path integration in more natural conditions. Unlike astronomical configurations and distant landmarks, our light source was close to the subjects. Therefore it moved across the hamsters' retina during translations as well as rotations and may have been difficult to use as a stable reference by the moving animal. Thus, our results do not completely rule out the possibility that, in nature, hamsters, which are active at night and dusk (Aschoff et al. 1973; Morin 1985), may depend on a temporary reference such as for instance the moon, the configuration of the night sky they are most likely to use on the basis of their weak visual acuity (Emerson 1980). The second question raised in this paper concerns the timing of the uptake of directional information from the light spot during one par-

39

Etienne et al.: Effect o f light cue on homing titular hoarding excursion. In our experimental conditions, the light spot seems to exert its full location-based effect provided that the hamsters can perceive it during a certain timespan (see experiment IC) at the arena centre, immediately before starting their return itinerary. As revealed by experiment IIC, the additional presentation of the light cue during the return itinerary exerts no influence either on the very rapidly occurring return from the centre to the periphery of the arena (Fig. 11), or on the duration of the search for the nest entrance (see above). The influence of visual feedback on a goalorientated trajectory has been analysed extensively in gerbils, Meriones unguieulatus. Provided the animals were allowed to initiate their itinerary with respect to an array of landmarks, they were able to reach the goal in darkness. They therefore must have planned their trajectory by taking into account not only its angular, but also its linear components (Collett et al. 1986). When tested with respect to moving landmarks, the gerbils' reliance on visual feedback depended on the complexity of the array of landmarks and its relation to the goal location (Collett 1987). Let us remember, in this respect, that in the present study the hamsters' return itinerary depended on a 'Sollwert' which pointed mainly in a direction opposite to that of the light spot. In a different test situation, where the intended homing direction was aligned with the position of the light cue, the hamsters seemed to use visual feedback to improve the precision of their return (unpublished data). Rather unexpected was the location-based influence of the light spot in experiment IIA1, where the familiar visual cue was presented from the beginning of the outward journey to the beginning of hoarding (see Fig. 9 and above). The homing vectors express a predominant influence of internal route-based information, but at the same time a significant deviation from the nest entrance which depends on the light spot as a location-based cue. The two control experiments IIA2 and IIB (see above and Fig. 10) suggest that the light spot exerts a location-based effect provided it has been presented for a sufficiently long time at the beginning of the hoarding excursion to catch the subjects' visual attention. Remember that the uptake of food at the centre of the arena lasts 25-30 s. Thus, there was a relatively long interval between the presentation of the spot and the beginning of the return itinerary.

(a)

(b)

(c)

9

O

9

O

12. Hypothetical computation of homing direction. (a) Experiment IBI, (b) experiment IIA and (c) experiment ID. The angular positions of the light spot before (o) and after (e) hoarding has been initiated are indicated. The hatched arrows indicate the hypothetical vector the subjects may have computed at the end of the outward journey; the continuous arrows represent the observed homing vectors. The curved arrows around each circle represent the shift in the homing vector which is supposed to occur during hoarding. Figure

The results of experiment IIA open up a number of questions as to the manner in which the hamsters compute the homing vector on the basis of the internal assessment of the outward journey and of a familiar visual landmark. In Fig. 12 we attempted to represent in a very hypothetical manner how this computation may evolve on an internal level of representation, which we may assume to exist within the animal's central nervous system. Three different experimental conditions are considered in which the spot appeared with a 90~ with respect to its standard position. In situation (a) the familiar spot is presented from the beginning of hoarding to the end of the return itinerary (experiment IB1); in situation (b) it is presented from the moment the animal leaves the nest until hoarding has been initiated (experiment IIA1); in situation (c) the spot appears in one angular location during the outward journey and is shifted to a second location at the beginning of the hoarding phase (experiment ID1). The arrows in each of the three circles represent two successive phases in the hypothetical determination of the homing vectors. In condition (a), the subjects walked in complete darkness to the arena centre; at the end of their outward journey, their route-based homing vectors must have pointed towards the nest entrance. Under the location-based influence of the light spot, which was presented under a clockwise shifted angle throughout the hoarding phase, the route-based vector is assumed to have undergone a clockwise shift. Thus, the observed homing vector points about 60 ~ away from the nest entrance.

40

Animal Behaviour, 39, 1

In condition (b), the light spot was rotated clockwise from its standard position and presented from the moment the subjects left the nest exit to the moment they initiated the hoarding phase at the arena centre. Had the subjects been induced to return immediately to their nest upon their arrival at the food source, without remaining at the arena centre for about 25 s, in complete darkness, they would most likely have returned in a direction that depended primarily on the light spot as a locationbased cue, and secondarily on the internal assessment of the outward journey. During hoarding, the relative weight of the location-based visual reference seems to have faded, thus enhancing the influence of internal route-based information. The resultant homing vector therefore expresses a predominant influence of self-generated information, and a secondary influence of the familiar visual reference. Finally, condition (c) involved the presentation of the light spot throughout the hoarding excursion, its position being shifted by 180~ at the end of the outward journey. So far, we have interpreted the homing direction observed in this experimental situation (ID) as expressing a compromise between the influence of internal route-based information and the location-based effect which the spot exerts when it is in its final position (see above). An alternative explanation of this result is based on the assumption that the light spot already exerts a location-based control during the outward journey. At the end of the outgoing trip, the intended homing vector would therefore point in a direction that expresses, as in condition (b), the predominant location-based influence of the light spot, and the secondary influence of internal route-based information. The subsequent shift of the spot carries with it the initial vector and thus leads to the observed homing vector. As the light spot has been presented in two completely opposed angular positions, the final homing vector deviates less from the nest entrance than the vector observed in condition (a). The results of experiments ID2 and ID3, however (see Figs 7 and 8), which also involved two successive shifts of the spot, are less compatible with this type of interpretation than the results of experiment ID1. An important conclusion to be drawn from experiment IIA concerns the location-based effect which the light spot exerts during its presentation at the beginning of the hoarding excursion. We may therefore assume that as soon as the animals

have become familiar with a stable reference from the outside world, they tend to use it throughout their hoarding trips as a location-based landmark. Only experiment IA (see Fig. 2) therefore provided conditions in which the light spot could potentially exert a purely route-based influence affecting the timing and processing of spatial information (see Wallraff & Sinsch 1988). Thus, our actual results do not justify a strict dichotomy between the route-based and locationbased use of spatial cues from the environment. The classification of spatial information which we have adopted throughout this research leads, like all classificatory attempts, to inconsistencies if we apply it too rigidly; it keeps its value as a working hypothesis, however, which helps us to analyse when and how spatial information is registered and processed within sequentially organized locomotor behaviour. ACKNOWLEDGMENTS This research was supported by the Swiss National Science Foundation (grant no. 3.753.0.80). Many thanks are due to R. Maurer and A. Kfouri for very helpful discussions and remarks concerning the manuscript, to S. Joris for evaluating the statistics of the results, to R. Schumacher for his much appreciated technical assistance, to J.-J. Meyer for measuring the luminescence within the experimental arenas, to W. Wiltschko and an unknown referee for valuable comments on the manuscript. REFERENCES Aschoff, J., Figala, J. & P6ppel, E. 1973. Circadian rhythms of locomotor activity in the golden hamster (Mesocricetus auratus) measured with two different techniques. J. comp. physiol. Psychol., 85, 20 28. Baker, R. R. 1984. Bird Navigation. London: Hodder & Stoughton. Batschelet, E. 1981. Circular Statistics in Biology. London: Academic Press. Collett, T. S. 1987.The use of visual landmarks by gerbils: reaching a goal when landmarks are displaced. J. comp. Physiol. A, 160, 109-113. Collett, T. S., Cartwright, B. A. & Smith, B. A. 1986. Landmark learning and visuo-spatial memories in gerbils. J. comp. Physiol. A, 158, 835 851. Durup, M. 1970. Etude exp~rimentale sur les capacit~s d'orientation et de localisation olfactiveschez le hamster dot6 Mesocricetus auratus Waterh. Marnmalia, 34, 18-33.

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(Received 26 May 1988; initial acceptance 16 July 1988; final acceptance 21 September 1988; MS. number: 3232)