ioral expression of hippocampal output, this second class of system properties must involve the process or processes through which learning-dependent information represented in the activity of hippocampal pyramidal cells ultimately is distributed to the motoneurons innervating muscles of the appropriate conditioned response. Although little is known about the interface between the hippocampus and motor systems, the available evidence suggests that such an interface is accomplished through: (a) a hierarchical organization of the brain's memory systems, whereby (b) output from the hippocampus is transmitted via projections involving the subiculum, retrosplenial cortex, and ventral pontine nuclei to modify fundamental stimulus-response relationships stored in the cerebellum; (c) output of the cerebellum then initiates or modifies activity transmitted along reflex pathways; (d) propagation time from the hippocampus to the cerebellum is sufficiently rapid to allow for a contribution of pyramidal cell output to currently executed behavior; (e) at least one of the neural structures efferent to the hippocampus (e.g., subiculum, retrosplenial cortex, anterior thalamus) may play a major role in determining whether or not learning-related activity in the hippocampus has a behavioral consequence.
In conclusion, the system properties of the hippocampus proposed here must be considered only initial characterizations in view of the very early stage of research in this area. Nonetheless, each of the properties identified represents a distillation of observations made by many different investigators using a variety of behavioral testing conditions. Together, they provide a critical set of constraints for further conceptualizations of hippocampal function, particularly those attempting a more formal characterization of hippocampal system properties through the study of network dynamics ( Barrionuevo et al., 1989; Berger et al., 1989; Brown et al., 1988; Harty et al., 1992; Levy et al., 1985; McNaughton & Morris, 1987; Rolls, 1986; Sclabassi et al., 1988a, 1989; Traub et al., 1987a,b).
Whatever models emerge from such research, they must incorporate properties capable of accounting for the principles of hippocampal function outlined here.
This research was supported by grants from the NSF (BNS-8843368), NIMH (MH00343), ONR (NO0014-87-K-0472), and AFOSR (89-0197). We also gratefully acknowledge Dr. German Barrionuevo and Dr. Donald Weisz for their helpful critiques of earlier versions of this chapter.
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