Placing hippocampal single-unit studies in a historical context.

A profound increase in the study of the role of the hippocampus in behavior and cognitive processing resulted from the startling discovery by O'Keefe and Dostrovsky in 1971 that hippocampal neurons fire selectively in different regions or ''place fields'' of an environment. That discovery spawned a comprehensive theory of hippo- campal function that was elucidated in the publication, The Hippocampus as a Cognitive Map by O'Keefe and Nadel in 1978. According to the theory, the hippocampus serves as the neural substrate for maps of allocentric space. The goal of this paper is to revisit the historical background for the development of the cognitive map theory and to examine the context in which the theory and the phenomenon of place field activity began to gain acceptance by the scientific community. While subsequent research has led some to question if the theory can adequately account for all consequences of hippocampal lesions and all the correlates of hippocampal cellular activity, it is clear the theory has stood the test of time and has been successful in generating an enormous amount of fruitful research. Hippocampus 1999;9:346-351. ! 1999 Wiley-Liss, Inc. In the 20 years since the publication of The Hippocampus as a Cognitive Map (O'Keefe and Nadel, 1978), the cognitive mapping theory has become one of the preeminent theories of hippocampal function in cognitive process- ing. The theory proposes that the hippocampus serves as the neural substrate for maps of allocentric space. Such maps free organisms from the confines of stimulus-response (S-R) interactions with the environment, and allow them to anticipate the existence of important stimuli from a distance. For instance, internal representations of the environment, or cognitive maps, allow organisms to avoid locations in the world where predators have been encountered, and to approach distant locations known to contain food, water, or mates. Since the publication of the theory, all new theories regarding hippocampal function in animals have been stated, by necessity, in juxtaposition to the cognitive mapping theory. Further, most studies investigating the effects of hippocampal lesions on behavior, or examining the behavioral correlates of hippocampal single-unit activity, are designed to test some facet of the cognitive mapping theory. Even when lesion and recording studies are not designed to directly address the cognitive mapping theory, the results are typically interpreted in light of it. The seed for O'Keefe and Nadel's theory was actually planted during the first half of this century with the work of E.C. Tolman. In the 1930s, when the central theme of American behavioral psychology was that all forms of knowing and understanding in rats and humans are merely the result of complex S-R or S-S conditioning, Tolman and his students espoused views that were much more in line with those of the Gestaltists than the Behaviorists. Tolman's observations of rats performing maze tasks led him to conclude that animals do not simply learn to complete such tasks on the basis of S-R relationships. He believed that rats learn to complete such tasks by creating and using maps of the environment. In his own words, ''In the course of learning, something like a field map of the environment gets established in the rat's brain'' (Tolman,1948). Such mapsrepresent the environ- ment as a configuration of elements, a gestalt, that allows the subject to navigate flexibly, approaching the food reward along the shortest route possible from any given location.