The hippocampus and space revisited

The hippocampal formation has long been the focus of in- tense interest among neuroscientists. The discovery by Sco- ville and Milner (1957) that the mesial temporal lobe, includ- ing the hippocampal formation, played a central role in memory function in humans can be said to have started the modern era of research on this brain system. There followed two decades of animal research aimed at creating experi- mental models of the memory defects observed in humans, including my dissertation research, which met with scant suc- cess (Nadel, 1968). Indeed, when John O'Keefe and I started considering the hippocampus and its possible role in spatial mapping several years later, one of our greatest challenges was to analyze the extant lesion literature in terms of this theory with the minimum amount of special pleading. There were already several hundred such studies, varying exten- sively in terms of exact size and regional location of the le- sion, the means by which the lesion had been created, the kind of animal used, the nature of the task, the kind of mo- tivation employed, and so on. Yet, it was our feeling in 1976, when we terminated the review of the lesion literature, which was ultimately published in The Hippocumpiis CIS a Cognitive Map (O'Keefe and Nadel, 1978), that the spatial hypothesis successfully handled the vast preponderance of these lesion studies as well as what was then known about the physiology of the hippocampal formation. In the years following publication of the book, most pub- lished lesion studies were concerned in some way with the spatial map hypothesis; most often, comparisons with rival hypotheses were involved. This was a frustrating period be- cause, although many thought they were testing our ideas, too frequently the major themes we hoped to stress were mis- construed. In this article I dig back into the book we pub- lished in 1978 and reiterate some of the themes that were important to us then, and remain so now. By so doing, 1 hope to bring out some of the reasons why we thought, and con- tinue to think, that space is so special as to warrant a structure as compelling as the hippocampal formation.