Space, the final hippocampal frontier?

It has been 13 years since O’Keefe and Nadel published their landmark theory on hippocampal function (O’Keefe and Nadel, 1978). They postulated that the hippocampus is critically involved in the formation of “cognitive maps,” which ultimately enable an animal to define its position within the environment. At the time their book was written, theories that explained hippocampal function did not sufficiently account for all the experimental findings, and their notion that the hippocampus processed spatiul memories appeared to be more consistent with the available data. Presumably, much of what prompted their theory was O’Keefe’s finding that single neurons in the hippocampus discharged only when an animal was located in a particular place in its environment (O’Keefe, 1976). H e referred to these cells as place cells, and the location from which they discharged was termed the place field. Since these initial observations, many laboratories have extended O’Keefe’s findings and have added a considerable body of knowledge concerning the properties of place cells. In recent years, a second type of spatial cell, the head direction cell, has been identified in the dorsal presubiculum (postsubiculum); these neurons discharge as a function of the animal’s head direction in the horizontal plane (Taube et al., 1990a). Although both of these spatial cells were originally identified in rodents, in recent years spatial cells in the hippocampus of nonhuman primates have also been observed (Rolls et al., 1989; Ono et al., 1989). While these neurophysiological studies are consistent with the cognitive mapping theory, it is important to consider the significance of these spatially tuned cells in terms of hippocampal function. This article will discuss whether the hippocampal formation is preferentially involved in spatial behavior by focusing its discussion on the following question: What d o the physiological recording studies on place cells and head direction cells tell us about hippocampal function? Along the way, comments will be made pertaining to some of the issues mentioned bv Nadel in his article.