An allocentric spatial model for the hippocampal cognitive map

The term “spatial behavior” is ambiguous and needs to be clarified. It might mean behaviors that can best be described with reference to a spatial reference framework. or it might mean behaviors that are dependent on spatial neural systems. An example of the first is the demonstration by Golani (1976) that the seemingly complcx movements which form the social interaction between two jackals can be described in several different frameworks, including the use of a framework centered on one animal to describe the movements of the other. Other aspects of behavior will best be described with reference to egocentric frameworks centered on the eye, head or body axis, or axes centered on individual objects or environmental frameworks. I t might transpire. however, that the neural systems that generate these behaviors are not in themselves spatial systems, but are acting according to nonspatial principles that conspire with the environment to produce “spatial” behavior. For example, the behavior of an animal approaching a light might best be described as reducing the linear distance between the animal and the object, but might in fact be subserved by systems operating on the principle “increase the intensity of the light,” resulting in the animal’s moving up an intensity gradient (Barto and Sutton. 1981). Similarly, as the behaviorists realized. even complex spatial behaviors such as maze learning could, in principle, be dependent on chains of simple associations between stimuli and responses (see stimulus A , activate muscle sequence I ; see stimulus B, activate muscle sequence 11, etc.). An example of the way in which a “nonspatial” hippocampus might support spatial behavior is the stimulus-response associationist model proposed by McNaughton (1988) and McNaughton and Nadel (1989). In this model the activity of the hippocampal complex-spike cells represents the sensory view from a location; the role of the hippocampus is to associate this view with a particular movement (e.g., turn left) in order to predict the subsequent local view. The power to generate novel behaviors on the basis of such a system depends on the ability to string together stimulus-response-stimulus components and to generate motor equivalences, such as two left turns are equivalent to an about-face in extrahippocampal areas like the parietal cortex. No spatial system is needed. The second meaning of spatial behavior is behavior generated by information stored in an explicitly spatial system. The strong claims of the cognitive map theory are that one such spatial system represents environments within an alloYIPPOCAMPUS, VOL. 1, NO. 3, PAGES 230-235, JULY 1991