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First published online March 22, 2004
Journal of Experimental Biology 207, 1491-1508 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00906
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Resetting the path integrator: a basic condition for route-based navigation

Ariane S. Etienne, Roland Maurer*, Valérie Boulens, Arik Levy and Tiffany Rowe

FPSE, Université de Genève, 40 Boulevard du Pont-d'Arve, CH-1211 Genève 4, Switzerland



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Fig. 1. Experimental room A and apparatus in experiment I. The rectangular room (567 cmx433 cmx220 cm) contained two arenas (diameter: 220 cm) that were equipped with a peripheral nest box. The short walls were either white or black with a grey margin, and the long walls were covered with two-dimensional landmarks. Three landmark objects were located between the two arenas. Normal room lighting was provided by lamps at floor level. An infrared video camera that was surrounded by a ring of infrared diodes (peak emission, 940 nm; bandwidth, 45 nm) was mounted on an optic bench and moved above the centre of the arena where the animal was being tested.

 


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Fig. 2. Test trials and expected homing directions in experiment I. The large circles with a small rectangle represent the experimental arena and peripheral nest box, respectively. The dotted arrows along the arena circle indicate that the arena has been rotated before the start of the trial. The continuous lines with an arrow within arena circles represent the outward journey to the food source. The small circles indicate that the animal walks in circles (diameter{approx}30 cm). Trials without a fix (left) take place under infrared light only, and the subjects can only home through path integration (PI) that is anchored to the current nest position (dotted arrows). In trials with a fix (right), the room lights are turned on for 10–12 s during or at the end of the outward trip, when the subject is located at P1. During a fix, the homing directions based on PI on the one hand, and on visual references on the other hand, diverge by 98°. The arrows starting at P1 or P2 represent the expected homing directions depending on PI that is reset by a visual fix (dashed arrows) or is not reset (dotted arrows). (In controlled reference trials, the two expected homing directions lead to the nest at 0°). In uncontrolled reference trials, the arena is not rotated and the animal is guided from the nest exit at 0° to any point on the arena floor, where it is offered food, and then returns to the nest. In controlled reference trials, the arena and nest box are rotated by 180° and then rotated back to the standard 0° position. From the nest exit at 0°, the hamster is led to one of five different locations (dots), where it walks along 2.5 full circles (small circle) in the dark, and then along a further circle in the opposite direction, the room lights being turned on. The animal is then offered food and returns home, in darkness. In both reference trials, homing is considered to be successful if the animal deviates by no more than 45° from the correct homing direction when reaching the arena periphery. Before the start of each experimental trial, the arena (with nest box) is rotated by 135° clockwise or counterclockwise. Only clockwise trials are presented here. In baseline trials, the hamster is guided to P1, where it picks up some food, and then to P2, where it fills its pouches completely and initiates the homing trip. Baseline-with-circling trials follow the same pattern, but the animal walks along 2.5 full circles near P1 instead of pouching food. In fix-without-translation trials, the animal is led to P1, walks along 2.5 full circles in the dark and then along a further circle in the opposite direction in the fully lit environment, fills its cheek pouches at P1 and returns towards the arena periphery. Fix-with-translation trials follow the same procedures; however, after the fix interval, the animal is led from P1 to P2, where it fills its pouches and starts the homing trip.

 


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Fig. 3. Evaluation of homing directions in experiment I. For each trial, the homing direction was measured in two coordinate systems. (A) The animal's position at the end of the homing trip, when it reached the 15 cm-wide peripheral annular zone of the arena (dashed circle) was coded with respect to the real arena floor, which was subdivided into 10° sectors. The 0° reference direction was the radius vector pointing from the centre of the arena to the standard nest location; positive values corresponded to clockwise angles. As the return to the nest (curved path) does not start at the arena centre, this measure entails a bias (see text). (B) The animal's orientation was therefore assessed by a second measure, at a distance of 35 cm from the start of the return, with a mobile grid (dotted circle), also subdivided into 10° sectors. The grid was centred on the start of the return at P2 (or P1), and its 0° reference direction was aligned with the standard position of the nest entrance.

 


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Fig. 4. Homing paths of one subject in the four classes of experimental trials of experiment I. The large circles represent the experimental arena with the nest box in its standard 0° position (dashed rectangle) and in its rotated position (continuous rectangle) during the experimental trials. The 15 cm-wide peripheral zone is shown by a dotted circle. The dashed lines (and circles) represent the outward journey to points P1 and P2. The return journeys from the feeding place at the end of the outward journey to the peripheral annular zone of the arena are drawn for the four different (clockwise and counterclockwise) experimental trials.

 


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Fig. 5. Mean homing direction of repeatedly tested subjects in experiment I (N=8). Each pair of large circles represents the arena in its clockwise (left) or counterclockwise (right) rotated position, and the two dashed lines inside are the two-leg outward journeys starting at the current position of the nest. The dashed rectangle beneath each circle represents the nest box in its standard 0° position, while the solid rectangle in the upper part of the diagram represents the rotated nest. The dots along the periphery of the arena circle indicate the mean orientation of each subject in 10–14 return trips, at the moment where the animal had reached the peripheral annular zone of the arena. The (larger) open circles on the same level represent the mean orientation of the whole experimental group. The arrows that are centred on the point of departure of the return journey represent the mean orientation of each subject at a distance of 35 cm from the starting point of the return. The mean orientation of the whole experimental group is represented by a large open arrow. For first order data, open symbols represent non-significant results and full symbols represent significant results (P<0.05 or 0.01; test of Rayleigh). All second order data are significant at the 0.01 level (test of Moore).

 


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Fig. 6. Geometry of test space and outward journeys in experiment II. The nest box is located under the arena floor, the nest exit (diameter, 9 cm) being located at a distance of 50 cm from the arena wall. The hamster can easily climb from the underground nest into the arena. Before each test trial, the arena is rotated by 135°. The outward journey (continuous line with heavy arrows) leads from the (rotated) nest exit (N135°) over 60 cm to point P1, and, with the exception of fix-without-translation trials, over a further translation of 110 cm to point P2. In baseline trials, the animal proceeds to P1, where it takes up some food, and then to P2, where it fills its cheek pouches completely. Baseline-with-circling trials follow the same pattern except that the subject walks along two full circles near P1 (circle passing through P1) instead of taking up some food. In fix-without-translation trials, the animal walks to P1, follows two full circles in the dark, and then a further circle in the opposite direction under light. Fix-with-translation trials include an additional translation from point P1 to point P2 after the fix. During the fix at P1, the nest direction, as established by visual cues on the one hand and by PI on the other hand, diverge by ~67°. A full resetting would lead to the standard nest location N0°, and a partial (direction only) resetting to the virtual nest location NDR. The theoretical homing directions based on a full or a partial resetting differ by 72° at P1 and by 125° at P2.

 


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Fig. 7. Mean homing directions of two subjects in experiment II. The homing directions are measured at a distance of 50 cm from the point of departure of the return. The mean return vectors (arrows) are superimposed on the outward trip to the food site (solid lines; circling not shown). The four vectors in each graph represent the homing directions of subjects 1 (solid arrows) and 2 (dashed arrows) in clockwise and counterclockwise trials. Vectors from counterclockwise trials are presented mirror-reversed. (Solid arrowheads, P<0.05; open arrowheads, P>0.05; test of Rayleigh.) Circle NDR represents the location of a virtual nest that would result from a partial resetting acting on the subject's azimuth only.

 


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Fig. 8. Return paths of subject 1 in experiment II. Only clockwise data are presented. Before the trials, the arena has been turned 135° clockwise. The filled circle represents the rotated position of the nest hole, the small black dot represents point P1, and the small open circle represents the standard location of the nest hole. The large open circle encompasses the starting point of the return trips. The return paths of subject 1 (N=11–14) are represented by a continuous line with an arrow and occasionally by a dashed line. The bottom graph illustrates a return path through trial-and-error exploration in a clockwise baseline trial by subject 2.

 

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© The Company of Biologists Ltd 2004