Animal cognition in the field and in the laboratory

During the first part of the XXth century, ethology was grown up an important research field, under the impulsion of Max Von Frisch, Konrad Lorenz, Robert Hinde or Niko Tinbergen, to cite just a few of the most famous ethologists. Two important European reviews, "Behaviour" and "Zeitschrift für Tierpsychologie" provided repertoires of animal adaptive strategies in natural conditions. These observations were mostly described in terms of inherited capacities to react to a given stimulus, thus promoting the view that adaptive behavior was mainly due to preprogrammed sequences triggered by appropriate stimuli or released by an internal innate mechanism. This exclusive alternative of internal innate representations of goal oriented behavior or of automatic responses to relevant external stimuli ruled out the possibility that animals might memorize representations of the environment.

In this perspective, the performance of squirrels retrieving buried nuts was mainly attributed to their insistence in digging at the basis of a vertical wall or cylinder, such as tree trunks, both for caching and retrieving food. If all the animals of the same species were sharing the same rule, it was supposed, an individual did not need to memorize where it had buried nuts. The probability to dig out a nut in such a standard context was relatively high, whether finding its own nuts or those cached by another squirrel. Thus, animals did not need projects or plans, just a perseverance in expressing innate stereotyped motor responses. This type of explanation was commonly accepted, even reinforced by the expected fundamental difference between animals and men.

Meanwhile, experimental psychologists such as Edward Tolman were working in the laboratory, observing Norwegian rats in mazes which they considered as the best substitute for their natural environment (tunnels or rubbish accumulations). In a famous paper dated 1948, Tolman described rats' orientation in mazes as implemented by a "cognitive map". He based his major argument on the rats' capacity to make a detour or a short cut in a slightly modified familiar environment. His main opponent was Clark Hull, who tried to analyze rats' sequence of choices in similar situations as emerging from the progressive binding of chains of stimulus responses. Eventually, the design used by Tolman was regarded as having obvious flaws, which helped rejecting the idea of a rat "lost in thoughts".

Thus, until the end of the seventies, it was hardly possible to find the word "memory" or "learning", even less the adjective "cognitive" in the titles of the papers reporting animal behavior experiments in neuroscience journals. However, two books published in 1978 made an outbreak. "The hippocampus as a cognitive map" by John O'Keefe and Lynn Nadel and "Cognitive processes in animal behavior" by Steward Hulse, Harry Fowler and Werner Honig. The first book was a real "pavé dans la mare" as it proposed that the hippocampus, a structure of the limbic system supposed to be man's hidden and despised heritage of animal brain, was implementing spatial cognitive maps "à la Tolman" in both animals and humans. It was supported by the development of electrophysiological recording in the hippocampus of freely moving rats revealing the existence of brain networks engaged in spatial representations (O'Keefe, 1976). The second book analyzed animal behavior as based on intentions and plans, thus providing a firm basis for the researchers interested in cognitive processing in animals.

One major weakness of this research line was that laboratory rats had been bred and selected for hundreds of generations and were moving in artificial laboratory environments, driven by artificially modified motivations. To some scientists, the results obtained from such experiments were as far from what could be expected from wild animals in their environment as were in vitro from in vivo experiments.

John Krebs, in Cambridge, contributed to bridging the gap during the early 80ies. He analyzed memory capacities from marsh tits, in the field and in aviaries in which the birds were allowed to cache food for later retrieval, depending on their motivation (Shettleworth and Krebs, 1982; Krebs, 1983). To make a long story short, this line of research illustrated the remarkable spatial memory capacities of different bird species and revealed that these capacities were positively correlated with the development and expansion of the hippocampus in food storing birds (Clayton and Krebs, 1995).

This last step provided a strong impulse to a new field of neuro-eco-ethology, in which scientists collected experimental laboratory and field observations linking the development and function of the hippocampus with a specialization in food caching and retrieval, both in birds and in mammals (Jacobs and Liman, 1991, Jacobs, 1995).

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