Exceptions to the rule of space

There are many points in Nadel’s paper with which we heartily agree. At a general level we most strongly agree that a good theory of hippocampal function should be explicit and unambiguous about the kind of information that the hippocampal formation is handling. As Nadel points out. many contemporary positions are limited by their inability to say anything plainly about this issue-they are limited in that they seem to make few clear predictions and seem to lack generality across species and behavioral paradigms. This has not been the case with O’Keefe and Nadel’s position. A key point that should not be lost is their assertion that the hippocampal formation is essential for place learning. that is, for situations in which the topographical relationships i n the environment come to guide an animal’s behavior. This was a very bold claim in the mid-1970s and, to the surprise of most of their contemporaries, the subsequent experimental record is basically unanimous-they were right. Repeatedly, in the hippocampal lesion literature using nonprimates the presence of a specific place learning requirement in a task. as opposed to, for example, working memory, temporary memory buffer. or other nonspatial requirements, has been shown to be critical in detecting a behavioral impairment. For those of us convinced of the basic correctness of this central assertion by O’Keefe and Nadel, more data demonstrating the existence of an intimate l ink between hippocampal circuitry and place memory do not further sprcjfictil1.v strengthen O’Keefe and Nadel‘s theorv. For example. the demonstrations that certain forms of spatial memory of birds are affected by damage that includes the hippocampal formation will not allow, by themselves, further elucidation of the specific contribution of hippocampal circuitry in solving spatial problems. The same holds for the association between variations in the size of hippocampal components and variations in performance in hippocampal-sensitive tasks. such as two-way active avoidance. These new data do not add a novel kind of support for O’Keefe and Nadel‘s explanation for ~ ’ h y the hippocampal formation is important for place learning. The nub of our story is this: O’Keefe and Nadel assert that instances of impaired learning and memory in animals with damage to the hippocampal formation are caused by the elimination of an explicitly topographical, mnemonic representation of the environment, that the kind of information that the hippocampal formation handles is necessarily spatial; we part company with them here. We have chosen a different, although not unrelated, path in accounting for the specific contribution that the hippocampal formation makes to learning and memory. On reviewing the hippocampal literature, we were impressed with two things: place learning is impaired after HPC damage, and there are several instances of impairments that do not appear to fit well with the idea that the hippocampal formation makes its special contribution to memory by constructing and storing spatial maps of the environment. We have already dealt in detail with these “exceptions” (Sutherland and Rudy, 1989). Nadel acknowledges that the last 15 years of experiments on the hippocampal formation have produced “a small number of exceptions” to his position. It is in this small, unassimilated fringe (which Nadel also acknowledges contains one of the human hippocampi), where we set up camp. We felt motivated t o find some way of characterizing the kind of information unique to the hippocampal formation so that both the place learning impairment and the “exceptions” could be explained in the same manner. I t was also important to us that our way of chara c t e r i h g hippocampal function should predict new behavioral situations in which hippocampal circuitry makes an essential contribution. We were also fortunate to have read Hirsh’s (1974) paper, which prompted us to believe that following the path we have chosen was not altogether unreasonable. Our position is that hippocampal circuitry is necessary if a problem cannot be solved on the basis of strengthening or weakening associations between elementary stimulus events, that is, if an animal must form associations between cue conjunctions and some other event. Topographical relationships are but one example of the many kinds of cue conjunctions or relationships that are possible. Essentially. the hippocampal formation enables an animal to disambiguate the significance of an elemental stimulus or cue when the meaning of that cue depends upon its relationship to one or more other cues. Place learning falls into the category of impaircd abilities precisely because if an animal must navigate to a specific location using topographical relationships among cues. then the way that an animal should move when it is facing any particular cue is ambiguous: the cue’s significance for guidance necessarily depends upon its relationship to some other element of the environment. starting location. other perceptible cues, etc. If the animal can solve the spatial problem by using only a single element of the situation t o guide its movements, then by definition this would require only it taxon strategy for solution, or, to use our terminology. a simple association solution. Nadel states quite clearly that he is not averse to the idea that one 01‘ the human hippocampi represents information that is more “abstract” than physical space. We are saying something similar about the hippocampal formation in both hemispheres of all species-primates to birds to fish. Species differ dramatically in the kinds of perceptual or motor information represented by activity in ensembles in neocortical zones and other structures that provide input to the hippocampal formation. ’Therefore, the kinds of cues or events that can enter into hippocampal-based configural associations may differ dramatically among species. Our view clearly predicts that it should be possible t o find examples of impaired configural memory after hippocampal damage, in addition to. and quite apart from, those involving spatial mapping-this search is of course hopeless if O’Keefe and Nadel’s theory is more in line with hippocampal function.