Crusio, Wim E. (1997) The hunting of the hippocampal function. Behavioral and Brain Sciences 19 (4) 767-768.
Commentary on Eichenbaum, H., Otto, T & Cohen, N. J. (1994) Two Functional Component of the hippocampal memory system. BBS 17 (3) 449.


The hunting of the hippocampal function

Commentary on Eichenbaum, H., Otto, T & Cohen, N. J. (1994) Two Functional Component of the hippocampal memory system. BBS 17 (3) 449

Wim E. Crusio

Génétique, Neurogénétique et Comportement
URA 1294 CNRS, UFR Biomédicale
Université Paris V René Descartes
45, rue des Saints-Pères
75270 Paris Cedex 06
France

Electronic mail: crusio@citi2.fr

Abstract

The present theory suffers from a lack of ecological validation. It is not at all clear why the hypothesized faculties would have evolved and what would be their adaptive value. I argue that hippocampal function can only be understood if the animal is seen in its natural context.



More than 120 years ago, Lewis Carroll (1992) wrote: 'Twas brillig, and the slithy toves / Did gyre and gimble in the wabe; / All mimsy were the borogoves, / And the mome raths outgrabe!

Many people admit to difficulties in understanding this admonishment, despite the fact that the next sentence reads: "Beware of the Jabberwock, my son!" Some might even say that all this is just gibberish. Of course, those who know better see that it is not. Why, then, are these phrases so difficult to understand? I think the main reason is that most people tend to forget that the above text was found by Alice in the land behind the looking-glass. From Alice's account it becomes exceedingly clear that this is a land with a whole set of customs and laws of its own, even natural laws being different there. It should therefore be obvious that the text cited above can only be understood in the context of the land behind the mirror. And indeed, although this text made no sense at all to Alice, it appeared completely sensible to Humpty Dumpty, one of the inhabitants of that land, enabling him to explain the text to Alice almost effortlessly.

What has this to do with the hippocampus? The analogy is clear: We can only hope to understand the hippocampus if we recognize that this structure is not functioning in a vacuum. The hippocampus is part of a brain, which is part of an organism, which is part of an ecosystem. The hippocampus has evolved, and has started to execute certain functions, as a consequence of selection pressures coming from the animal's ecological surroundings. Therefore, in order to explain successfully what the hippocampus does, theories will have to take these aspects into account. One of the implications may well be that, depending on a species' specific ecology, hippocampal function may differ to some extent between species (see also Shettleworth, 1993). In fact, hippocampal anatomy, perhaps in response to specific selective pressures, is known to differ extensively between species (Clayton & Krebs, 1995).

Eichenbaum et al.'s (1994) target article provides a well-informed account of many characteristics of the hippocampus. Nevertheless, the reader gets the distinct impression that what species is being studied -rats, mice, monkeys, humans- really does not matter much. I think it does: this aspect may even be crucial. For example, Olton et al. (1979) distinguished between working and reference memory. Although these concepts may be valid for rats (and perhaps humans), it is doubtful whether they are valid for mice, as well (Crusio et al., 1993).

Inter-species differences are not the whole story, however. A well-known phenomenon is the occurrence of large interindividual differences in hippocampal anatomy and chemistry within one and the same species (Lipp et al., 1989; van Daal et al., 1991). To a large extent, such differences are heritable (Crusio et al., 1986; Van Daal et al., 1991)1 and have considerable consequences for an animal's behavior (Lipp et al., 1989; Crusio et al., 1993). To the best of my knowledge, none of the existing theories on hippocampal functioning take the phenomenon of interindividual variation into account, let alone try to explain it. Eichenbaum et al.'s (1994) hypothesis is no exception.

Although not completely satisfactory, until now the most successful theory of hippocampal functioning is O'Keefe and Nadel's (1979) cognitive mapping theory (see also Nadel, 1991, and accompanying commentaries). An important reason for its popularity is, I think, that their theory is in large part firmly rooted in ecological theory. To arrive at a deep understanding of the hippocampal function, we should start to look at the animal in its natural environment. I challenge Eichenbaum et al. (1994) to indicate what the particular survival value might be -for an animal in its environment- of what they think the hippocampus is doing. In addition, I would be interested in any speculation they can offer us regarding the interindividual variation referred to above.

In sum, my main critique of Eichenbaum et al. (1994) is that they ignore the above questions completely. The question of ecological validity was also raised by Bingman (1994) and Nadel (1994), but I don't feel that it has been adequately answered. In their reply (par. R2.6), Eichenbaum et al. (1994) comment on ecological aspects of the spatial mapping theory, but not on those of their own hypothesis. I think the presented hypothesis should be framed in a more ecological context. Ignoring ecology might easily put us, when the hunting for the hippocampal function is over, in a position reminiscent of the Baker's, who experienced that, after all, the snark was a boojum (Carroll, 1992).

Note

  1. It should be stressed here that this concerns natural, normal, non-pathological variation between individuals.

References

Bingman, V. P. (1994) Remembering spatial cognition as a hippocampal functional component. Behavioral and Brain Sciences 17:473-474.

Carroll, L. (1992) Alice in Wonderland. Unabridged edition containing a.o. Alice's Adventures in Wonderland (1865), Through the Looking-Glass (1872), and The Hunting of the Snark (1876). Wordsworth Editions Limited, Hertfordshire.

Clayton, N. S. & Krebs, J. R. (1995) Memory in food-storing birds: from behaviour to brain. Current Opinion in Neurobiology 5:149-154.

Crusio, W. E., Schwegler, H. & Brust, I. (1993) Covariations between hippocampal mossy fibres and working and reference memory in spatial and non-spatial radial maze tasks in mice. European Journal of Neuroscience 5:1413-1420.

Eichenbaum, H., Otto, T. & Cohen, N.J. (1994) Two functional components of the hippocampal memory system. Behavioral and Brain Sciences 17:449-518.

Lipp, H.-P., Schwegler, H., Crusio, W.E., Wolfer, D., Leisinger-Trigona, M.-C., Heimrich, B. & Driscoll, P. (1989) Using genetically-defined rodent strains for the identification of hippocampal traits relevant for two-way avoidance learning: A non-invasive approach. Experientia 45:845-859.

Nadel, L. (1991) The hippocampus and space revisited. Hippocampus 1:221-229.

Nadel, L. (1994) Hippocampus, space, and relations. Behavioral and Brain Sciences 17:490-491.

O'Keefe, J. & Nadel, L. (1979) Précis of O'Keefe and Nadel's "the hippocampus as a cognitive map". Behavioral and Brain Sciences 2:487-533.

Shettleworth, S. J. (1993) Varieties of learning and memory in animals. Journal of Experimental Psychology: Animal Behavior Processes 19:5-14.

van Daal, J.H.H.M., Jenks, B.G., Crusio, W.E., Lemmens, W.A.J.G. & van Abeelen, J.H.F. (1991) A genetic-correlational study of hippocampal neurochemical variation and variation in exploratory activities of mice. Behavioural Brain Research 43:65-72.