Limitations in the Assessment of Path Dependent Information

Abstract

When hoarding food in an experimental arena (ø = 2.20 m), golden hamsters tend to return along a direct path from the food source at the centre of the arena to their peripherally located nest. Under infra-red light the animals' homing behaviour is exclusively controlled by 'internal' cues which have been generated during the outward journey to the feeding place. The paper examines the limitations on the registration and computation of directional cues which originate from an active or a passive outgoing trip. The compensation of the angular component of the outward journey was examined by inducing the subjects to walk (actively) around the centre of the arena, or by rotating the animals (passively) on a platform which contained the food source. The greater the number of rotations, the less precise the homing performance. After three to five active rotations, and after two to three passive rotations of 360°, the animals ceased to yield significant homing vectors. Unidirectional rotations induced a systematic ipsidirectional bias, an indication of undercornpensation; no bias was observed after rotations which occurred in equal extents in both directions. Special importance was given to the compensation for passive translations. The experiments involved either the shift of the subjects from their nest exit to an unfamiliar, adjacent arena, or the combination of an active and a passive outward leg during the outward journey to the centre of the animals' own arena. During their return to the nest, either the hamsters did not take into account at all the direction of the passive translation, or if they did, the compensation was only limited. These results are discussed in relation to the animals' capacity to assess 1) an active outward journey through the availability of different categories of self generated cues, and 2) a passive outward journey predominantly on the basis of vestibular signals. A final series of experiments showed that under certain conditions, the hamsters commit systematic homing errors which can be attributed to their failure to initiate the registration and computation of path dependent cues at the right instant in time and space

Path integration in mammals

“…During active walking without vision, the assessment of path length depends less on inertial information than on nonvestibular motion cues, such as proprioceptive feed back and efference copies. This has been observed in rodents, which update their position much more accurately during actively performed translations than during passive shifts (Mittelstaedt and Mittelstaedt, 1982;Etienne et al, 1988). Similar conclusions can be drawn from experiments on normal (Mittelstaedt and Mittelstaedt, 2001) and labyrinthine-defective (Glasauer et al, 1994(Glasauer et al, , 1999 human subjects who had to estimate and reproduce the length of a path or to cover the distance to a previously seen visual target.…”

“…Furthermore, PI being an incremental recursive process, in which changes in the current estimate of the position are added to the position vector of the previous step, these errors are necessarily cumulative (Etienne et al, 1988). Benhamou et al (1990) therefore added an explicit representation of Gaussian noise to a trigonometric formulation of PI (Benhamou et al, 1990).…”

“…Strategies for such masking include testing the animal under infrared (IR) light or surrounding the testing environment with undifferentiated walls, and cleaning the surface of the apparatus so as to render olfactory cues ineffective. The second method is to set external cues and PI in a twofold (Etienne et al, 1986(Etienne et al, , 1988 or threefold (Etienne et al, 1990) conflict with each other. In such conflict situations, if an animal relies on selfmotion cues, it should behave according to these rather than according to references from the proximal and/or distal environment.…”

“…Among the latter, inertial signals from the semicircular canals play a specific role in assessing angular motion. This has been shown by experiments in which rodents (Mittelstaedt and Mittelstaedt, 1982;Etienne et al, 1988) and humans (Metcalfe and Gresty, 1992;Israel et al, 1995) had to reproduce or compensate for passive rotations around their vertical axis. Angular velocity, the output of the semicircular canals, is time-integrated at a higher level of the nervous system to allow the subject to estimate its heading (Israel and Siegler, 1999).…”

“…During active walking, proprioceptive and further cues from locomotion complement vestibular information. For example, hamsters update direction more accurately, and over a larger range of rotations, when they walk actively around a foraging site than when they are rotated on a platform where they collect food items (Etienne et al, 1988).…”