Articles

Time-Dependent Processes in Memory Storage

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Science  16 Sep 1966:
Vol. 153, Issue 3742, pp. 1351-1358
DOI: 10.1126/science.153.3742.1351

Abstract

These observations indicate that the long-lasting trace of an experience is not completely fixed, consolidated, or coded at the time of the experience. Consolidation requires time, and under at least some circumstances the processes of consolidation appear to be susceptible to a variety of influences— both facilitating and impairing— several hours after the experience. There must be, it seems, more than one kind of memory trace process (31). If permanent memory traces consolidate slowly over time, then other processes must provide a temporary basis for memory while consolidation is occurring. The evidence clearly indicates that trial-to-trial improvement, or learning, in animals cannot be based completely on permanent memory storage. Amnesia can be produced by electroshock and drugs even if the animals are given the treatment long after they have demonstrated "learning" of the task.

Of particular interest is the finding that retention of the inhibitory avoidance response increases with time. In a sense this should be expected, for it has long been known (and ignored) that, within limits, learning is facilitated by increasing the interval between repeated trials (7, 30). Our result may be the simplest case of such an effect. Since the improvement in retention with time seemed not to be due solely to consolidation (as indicated by electroshock effects), it would seem that the "distribution of practice" effect, as it is typically designated, may be due in part to a time-dependent temporary memory storage process. In our work with animals we have found no analog of human immediate memory such as that required for repeating digits (or finishing sentences). Animals tested immediately on the task described above after a trial typically showed no evidence of memory. It could be that the poor performance is due to excessive fright, but the "distribution of practice effect" is also typically observed in learning experiments in which food reward is used rather than shock avoidance. Since the retention tasks require the animals to change their behavior in some way, it could well be that the growth of retention over the first few minutes after a trial is due to time dependent processes involved in the organization of processes necessary for changing behavior, in addition to those involved in temporary storage and retrieval. It is worth pointing out that there is evidence of an analogous process in human memory (32).

A complex picture of memory storage is emerging. There may be three memory trace systems: one for immediate memory (and not studied in our laboratory); one for short-term memory which develops within a few seconds or minutes and lasts for several hours; and one which consolidates slowly and is relatively permanent. The nature of the durability of the longterm memory trace (that is, the nature and basis of forgetting) is a separate but important issue. There is increasing evidence and speculation (20, 21, 33) that memory storage requires a "tritrace" system, and our findings are at least consistent with such a view.

If there are, as seems possible, at least three kinds of traces involved in memory storage, how are they related? Is permanent memory produced by activity of temporary traces (31), or are the trace systems relatively independent? Although available findings do not provide an answer to this question, there does seem to be increasing evidence that the systems are independent. Acquisition can occur, as we have seen, without permanent consolidation, and both short-term and long-term memory increase with time. All this evidence suggests (but obviously does not prove) that each experience triggers activity in each memory system. Each repeated training trial may, according to this view, potentiate short-term processes underlying acquisition while simultaneously enhancing independent underlying long-term consolidation. Obviously, acceptance of these conclusions will require additional research.

If this view is substantially correct, it seems clear that any search for the engram or the basis of memory is not going to be successful. Recognition of the possibility that several independent processes may be involved at different stages of memory may help to organize the search. A careful examination of the time course of retention and memory trace consolidation, as well as examination of the bases of the effects of memory-impairing and memory-facilitating treatments, may help to guide the search. It is clear that a complete theory of memory storage must eventually provide an understanding of time-dependent processes in memory.

In 1930 Lashley wrote (2), "The facts of both psychology and neurology show a degree of plasticity, of organization, and of adaptation and behavior which is far beyond any present possibility of explanation." Although this conclusion is still valid, the current surge of interest in memory storage offers hope that this conclusion may soon need to be modified.

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