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insensitive to ISI while instrumental learning is not s. Isn't this simply additional evidence that the olfactory memory system of the rat is different from that involved in instrumental learning?

Learning-sets Reid and Morris not only fail to find evidence for learning-sets in the learning of novel odor discriminations, they are also unable to replicate earlier reports 1°'11 of reversal-set learning. In contrast, reversal performance in our experiments improved very quickly over three or four odor pairs. The noodor control procedure recommended by Reid and Morris 12 yielded no evidence of experimental artifacts (Staubli, U., unpublished observations). We also routinely (though not always) found above chance performance on trials 2-5 in odor discrimination learning, while Reid and Morris do not. These discrepancies raise the possibility of significant procedural differences between various odor learning experiments. Thus, while the criticisms and results of Reid and Morris provide good reasons to question the ability of the rat to form olfactory learning-sets, they also remind us of the need to directly compare paradigms when evaluating conflicting results in behavioral experiments. Where to go from here? Explaining the differences in experimental findings just mentioned and testing the criteria for learning-sets described by

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Reid and Morris are obvious steps. But independent of this, rats do appear to use experience-based procedures to encode olfactory information into a system with striking similarities to human recognition memory. It is too early to say if the rhinencephalon will rise again, but the road from rat brain anatomy to simple forms of human memory seems open.

Selected references 1 Lynch, G. (1986) Synapses, Circuits and the Beginnings of Memory, MIT Press 2 Tulving, E. (1984) Elements of Episodic Memory, Oxford University Press 3 Staubli, U,, Fraser, D., Faraday, R. and Lynch, G. (1987) Behav. Neurosci. 101,757-765 4 Milner, B. (1972) Clin. Neurosurg. 19, 421-446 5 Eichenbaum, H., Fagan, A. and Cohen, N. J. (1986) J. Neurosci. 6, 1876-1884 6 Staubli, U., Fraser, D., Kessler, M. and Lynch, G. (1986) Behav. Neur. Biol. 46, 432-444 7 Staubli, U., Ivy, G. and Lynch, G. (1984) Proc. NatlAcad. Sci. USA 81, 5885-5887 8 Slotnick,B. M. and Katz, H. M. (1974) Science 185, 796-798 90'Keefe, J. and Nadel, L. (1978) The Hippocampus as a Cognitive Map, Oxford University Press 10 Nigrosh,B. J., Slotnick, B. M. and Nevin, J. A. (1975)J. Comp. PhysioL PsychoL 89, 285-294 11 Slotnick, B. M. and Kaneko, N. (1981) Science 214, 91-92 12 Reid, I. C. and Morris, R. G. M. (1992) Proc. R. 5oc. London Ser. B 247, 137-143

Variations on our theme Reply by lan C. Reid and Richard G. M. Morris 'We might fairly gauge the future of biological science, centuries ahead, by estimating the time it will take to reach a complete, comprehensive understanding of odor' (Lewis Thomas, 1983) 1. The main aim of our article was to expose certain ambiguities inherent in the often repeated claim that rats acquire a learning-set during a short series of novel olfactory discrimination problems and to show that, when set against appropriate formal criteria, the claim cannot be substantiated. We are relieved that Hall agrees with our analysis ('they are surely right') and points out that, if anything, we have understated our case given that there is no necessary reason why perfect trial 2 performance should be taken to reflect the operation of some cognitive strategy. We agree. Lynch and Staubli also concede that we have provided 'important evidence against the proposition that learning-sets are responsible for the progressive improvement across successive discriminations'. A particularly crucial observation in our experiment was that a group of animals given successive reversals that demonstrably failed to acquire a strategy showed, nonetheless, just as an effective transfer to a novel problem as groups whose performance indicated that they might have learned a cognitive strategy. This result is all the more striking for the fact that the mean level of performance in our transfer problem was comparTINS, Vol. 16, No. 1, 1993

able to, if not better than, that reported for groups of animals elsewhere in the literature. That rats learn olfactory discriminations rapidly is not disputed; but the remarkable claim that rats acquire a true learning-set with odours several hundred times faster than do rhesus monkeys with visual cues remains unproven. Eichenbaum and Otto take a different view, claiming that they have used the phrase learning-set 'without prejudice about the underlying mechanisms '2. They are, of course, at liberty to use the terminology of learning-sets in a manner distinct from that in which it has been used classically (our difference of opinion is not semantic). What they are not at liberty to do is, thereafter, to refer to the term learning-set as if they have adopted the stricter definition. For example, although here chiding us for using only seven problems, Eichenbaum et a/. 2 claimed that olfactory learning-set formation in the rat is 'completely acquired' after three problems, more recently that it is apparently 'indistinguishable from that of primates 3 and that within this appropriate stimulus modality, rats can learn 'complex abstract rules '3. Clearly Eichenbaum and Otto are not using the term learning-set without prejudice to the underlying mechanisms and, interested as we and others are in the possibility that rats can learn abstract rules, we take issue with the claim that they do so after a short series of olfactory problems.

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A with B in addition to the individual odour-reward associations. Rats with hippocampal dysfunction should be unable to perform this relational comparison between the odours although they would still learn the odour-reward pairings (which the results of their successive discrimination task imply that they canS). Interestingly, Eichenbaum et al.'s own data fail to support this prediction because, paradoxically, it is their control animals that are unaffected by mispairing of odour pairs (e.g. when A + is paired with D - ) , while fornix lesioned rats are severely impaired 5. Eichenbaum's interpretation of these data in terms of 'encoding flexibility' refers to an important aspect of declarative memory but seems too ill-defined to allow confident predictions. We submit that, despite several ingenious experiments by both Eichenbaum's and Lynch's groups, the task of identifying precisely what type(s) of processing olfactory information entering the hippocampus can engage remains an enigma. The nose may be two synapses away from the hippocampus but we remain some steps from an answer.

Lynch and Staubli's point that the rationale for using olfactory learning rests as much with the unusual anatomy of the olfactory projections to the hippocampus as with the cognitive strategy issue is a very important point that certainly should be pursued in further research. The constructive point of our critique (with which we hope none of the participants in this debate would take issue) is that there are several distinct ways in which olfactory information could be being processed. Olfactory stimuli could, to take but one example, be providing information about the context in which other events or stimuli occur (e.g. the smell of apple pie reminding us of grandmother). However, experiments examining the formation of odour-reward associations alone are not the right way to model this; the contextual dimension has to be considered ~. Recently, Eichenbaum has proposed an intriguing 'relational processing' hypothesis of hippocampal function. The notion here is that the hippocampus engages in a process of comparing one stimulus with another and that a training paradigm like simultaneous discrimination learning encourages 'relational processing' because it provides an opportunity for the animal to move back and forth comparing the two concurrently presented odours. Clearly this would be more difficult in a successive discrimination procedure because of the additional burden of using short-term memory. The hypothesis therefore predicts that, in simultaneous discrimination tasks in which one odour is rewarded and another nonrewarded (A+, 13-; C+, D-; etc), normal animals will form representations of the pairing of

Erratum

In the November issue of TINS (Vol. 15, pp. 456-457) the identification keys to the graphs illustrating the results of Rallpack reports for the programs NEURON and GENESIS in the article by U. S. Bhalla, D. H. Bilitch and J. M. Bower were transposed. The correct verson is printed here. We apologise to the authors and to the readers for this mistake.

1 Thomas, L. (1983) Late Night Thoughts on Listening to /Hah/er's Ninth Symphony, Viking Press 2 Eichenbaum, I-t. E., Fagan, A. and Cohen, N. J. (1986) J. Neurosci. 6, 1876-1884 3 Otto, T. and Eichenbaum, H. E. (1992) in The Science of O/faction (Chobor, K. L. and Serby, M, eds), Springer-Verlag 4 Good, M. and Honey, R. C. (1991) Behav. Neurosci. 105, 499-509 5 Eichenbaum, H. E., Mathews, P. and Cohen, N. J. (1989) Behav. Neurosci. 103, 1207-1216

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