Behavioral and neural mechanisms by which prior experience impacts subsequent learning
Introduction
The neurobiological study of learning and memory has made significant progress in identifying the cellular and molecular mechanisms that support the acquisition and consolidation of long-term memory (Helmstetter et al., 2008, Johansen et al., 2011, Kandel, 2012). In addition, the essential neural circuitry underlying many of the model systems used to study learning and memory has been identified (Davis, 1997, LeDoux, 2000, Thompson and Kim, 1996, Tovote et al., 2015). However, one domain in which we have a relatively poor understanding of learning and memory function is how prior experience affects subsequent learning. This is a product of the fact that many neurobiological studies of memory employ experimental designs wherein the learning event is short-lasting and presented in isolation from prior experimentally-controlled events. This standard approach has its benefits in that the learning event can be clearly defined and controlled by the experimenter, however it comes at the expense of understanding how prior experience affects subsequent learning. Outside of the laboratory memory formation does not occur in a vacuum (Dudai, 2009), but instead occurs upon prior and ongoing experience. Understanding how past experience impacts later learning is essential for a better understanding of learning and memory processes.
Although much of the extant work on the biological basis of memory has not considered how prior experience affects subsequent memory formation, there is an evolving literature that has revealed that the prior history of an organism has a profound effect on future learning. This literature has fallen under the rubrics of synaptic tagging and capture, metaplasticity, and memory allocation (Hulme et al., 2013, Rogerson et al., 2014, Viola et al., 2014). While they have been labeled using different nomenclature, what they share in common is that they all describe conditions by which prior behavioral experience can influence subsequent learning. In what follows, I will describe findings from behavioral studies of metaplasticity, synaptic tagging and capture, and memory allocation. Special emphasis will be placed on comparing both the behavioral and neurobiological mechanisms that permit past events to influence subsequent learning. By doing so, I hope to offer insight into the processes that govern whether prior experience affects subsequent learning. While the focus of this review will be limited, the reader should note that a larger literature exists that describes a similar tendency for past events to influence subsequent learning. This includes the effects of stress on subsequent learning (Kim and Yoon, 1998, Schmidt et al., 2013), reactivation-dependent modification of memory (Finnie & Nader, 2012), and assimilation of new information into existing schemas (McKenzie and Eichenbaum, 2011, Tse et al., 2007, Tse et al., 2011).
Section snippets
Prior behavioral experience regulates subsequent learning
If the goal of the study of learning and memory is to understand how organisms adapt to ongoing and future experience, then experimental paradigms used in the laboratory must allow for the rigorous examination of how prior experience affects subsequent memory formation. While much of prior work examining the neurobiological mechanisms of learning have not taken this important consideration into account, recent studies on metaplasticity, synaptic tagging and capture, and memory allocation have
Neural mechanisms by which prior experience facilitates subsequent learning
Discussion of the neural mechanisms involved in behavioral studies of metaplasticity, memory allocation, and synaptic tagging and capture is complicated by the fact that in many of the experiments the nature of initial experience differs greatly across studies (e.g. cued fear conditioning versus spatial exploration), and in most cases, the antecedent and subsequent events also differ within experiments. Moreover, in the behavioral studies of synaptic tagging and capture the temporal order of
The time course by which prior experience affects subsequent learning
Early on in the experimental analysis of learning and memory it became apparent that the interval of time between learning trials is a critical factor in determining whether information is committed to long-term memory (Carew et al., 1972, Ebbinghaus, 1885/1913, Fanselow and Tighe, 1988, Josselyn et al., 2001, Philips et al., 2013). Trials distributed over longer periods of time produce better learning compared to trials spaced closely together, thus it is not unexpected that the interval of
A priming mechanism as a component of the memory trace
The data reviewed here suggest that there might be at least two mechanisms by which prior experience is able to impact later learning. The first is a mechanism whereby facilitation occurs when one event takes place within the time window of molecular consolidation engaged by a separate experience, akin to synaptic tagging and capture. The second type being the product of a longer lasting priming mechanism, possibly associated with learning related changes in intrinsic neuronal membrane
Conclusions
The studies reviewed here make it clear that prior experience has a profound effect on subsequent learning. The propensity of prior experience to influence later learning likely reflects an essential mechanism in the brain that balances the need to maintain the stability of networks that store information with the requirement that those networks also exist in a plastic state that allows them to adapt to future stimulation (Abraham & Robins, 2005). Given that memories are not formed in isolation
Acknowledgements
The author reports no biomedical financial interests or potential conflicts of interest. This work was supported by funds from Stony Brook University.
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2018, Behavioural Brain ResearchCitation Excerpt :This includes the effects of stress on learning, that has been the topic of considerable study [7], and various well-characterized conditioning phenomena [8–10]. In more recent years studies have started to describe additional conditions by which recent experience can affect the acquisition of memory [11]. One line of research includes a set of behavioral findings that confirm many of the predictions of the synaptic tagging and capture model [12].
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