Performance of goldfish trained in allocentric and egocentric maze procedures suggests the presence of a cognitive mapping system in fishes

Abstract

Goldfish were trained to obtain food in a four-arm maze placed in a room with relevant spatial cues. Four experimental conditions were run: allocentric, egocentric, egocentric + allocentric, and control. Relative to controls, all groups were able to solve the different tasks with high accuracy after 1 week of training. Subsequent transfer tests revealed place and response strategies for allocentric and egocentric groups, respectively, and both types of strategies for the ego-allocentric group. Moreover, the allocentric group showed the capacity to choose the appropriate trajectory toward the goal, even from novel starting points, presumably by using the distal cues as a whole. The results suggest that, in addition to using egocentric strategies, goldfish are able to solve spatial tasks on the basis of allocentric frames of reference and to build complex spatial cognitive representations of their environment.Fishes travel across a wide range of distances with surprising efficiency, whether in intercontinental migrations or on excursions within their habitual living areas. These travels indicate remarkable spatial abilities of fishes in navigating, orienting themselves, piloting, and recognizing their environment. Research in this field has been focused mainly on the innate fixed patterns of behavior and on sensory, ecological, and zoological factors. What seems to be underestimated in this research, though, is the possibility that spatial behavior is a flexible process that involves learning and memory mechanisms and cognitive phenomena (for a review, see Dodson, 1988). Such mechanisms are indicated by a number of naturalistic and experimental studies, such as the pioneer work of Aronson (1951Aronson ( , 1971) that showed that the gobiid fish Bathygobius soporator uses learned information about the spatial relationships of tide pools, or topographical memories acquired during exploration, to orient itself accurately. In fact, complex spatial learning and memory capabilities in fishes can be inferred from recent naturalistic studies

Place versus response learning in fish: a comparison between species

“…Such methods do, 55 however, lack flexibility, particularly in response to changes within the 56 environment, meaning the individual will be less likely to reach their desired 57 location from a novel start point (Rodriguez et al 1994). 58 O'Keefe and Nadel argued that animals are also able to navigate using 59 another set of processes which, although more cognitively demanding, are 60 able to adapt more readily to changes within the environment (O'Keefe & 61 Nadel 1978; Rodriguez et al 1994). These are called "allocentric processes".…”

Fish can encode order in their spatial map

“…However, the brain circuits involved in spatial cognition appear to be homologous to those of birds and mammals (Broglio et al 2003) and so it would be expected that spatial behaviour in fishes would be as complex as that in land vertebrates. There is evidence that fishes can encode information about their surroundings into a cognitive map (Reese 1989;Teyke 1989;Rodriguez et al 1994). The critical question is how they are able to form a map that is spatially larger than the fish's perceptual range.…”

Place and cue learning in turtles

“…Blanc, 1996). Hence, mammals and birds that rely on such an allocentrically referenced topographic representation of their environment can navigate accurately toward a place from different directions and adopt shortcuts and novel routes from places previously unvisited, even in the absence of local cues (Bingman, 1992;Gallistel, 1990;Nadel, 1991;O'Keefe & Nadel, 1978;ThinusBlanc, 1996; see also, for fishes, Rodriguez, Duran, Vargas, Torres, & Salas, 1994). Another remarkable property of navigation based on cognitive mapping is that it is resistant to the partial loss of relevant information.…”