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A neuroanatomic perspective on state‐dependent learning: The role of the striatum

The phenomenon of state-dependent learning (SDL) has both intrigued and frustrated investigators attempting to delineate the conditions under which such context-dependent encoding and retrieval dissociations can be demonstrated. Although originally and most consistently demonstrated with pharmacologic alterations in state by agents such as cholinergic antagonists ( l ) , marijuana, and ethanol (2), the concept has grown in theoretical breadth through the demonstration of similar dissociations in connection with exogenous and endogenous alterations of neural ”state”. State-dependent learning effects have been produced by electroconvulsive shock and kindled collvulsions (3), cortical spreading depression (4), exogenous and endogenous alteration in hormonal state (5 ) , alterations in drive state (6), time of day (7), sleep architecture (8), and mood state (9). (See Overton (10) for an extensive review of such studies.) To date, most conceptions of state-dependent phenomena have been phenomenologic in character. As outlined by Weingartner and co-workers (9), experienced events are encoded in an information context that determines which stimulus characteristics are attended to and selected as sigolficant and also the degree to which they are elaborated or processed. Retrieval strategies are similarly affected by an information context which determines how an information field is searched and a particular experiential event accessed. Most state-dependent dissociations are in effect context-dependent retrieval deficits since successful retention of material can be demonstrated with appropriate use of alternative strategies. The heuristic benefit of such a model for more general theories of memory can be seen in John’s (11) proposal that recall of a learned task is due to three separate neural circuits: One encoding the stimulus characteristics present at the time of original learning, a second encoding the context upon recall, and a third comparing the neural activity of the other two in order to determine if a response was indicated on the basis of similarity. It should be noted, however, that state-dependent paradigms have not in and of themselves generated any new understanding of memory deficits in clinical populations or of the biology of memory processing itself. Even in reviews of ”neurologic” theories of state-dependent learning, brain state and drug receptor state are referred to in a generic fashion, with little attempt made to identify the particular structures and substances that might be relevant to such phenomena. Is it even possible to relate specific neuroanatomic systems to such disparate conceptions of brain state and their effect on basic information processing? The answer to this question depends on the breadth of conceptualisation imbedded in the term ”state dependency”. One approach would be to study the phenomenon at its most basic level of expression in the central nervous system. Since movement is essential to the analysis of behaviour, investigation of the processes (i.e., ”preparatory set”) by which a given stimulus can differentially affect seemingly fixed motoric responses can be considered a study of ”state dependency” (12). Animal studies which have demonstrated differential cue use in pharmacologic manipulations of state have implicated alterations in the process of sensorimotor integration rather than simple response initiation loss (13). Whatever neuronal system was involved would certainly have to receive broad input from association cortex and have relatively direct connections with areas subserving motor output. Because the mes-