Commentary
Does assimilation into schemas involve systems or cellular consolidation? It’s not just time

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Abstract

A comment by Rudy and Sutherland [Rudy, J. R., & Sutherland, R. J. (2008). Is it systems or cellular consolidation? Time will tell. An alternative interpretation of the Morris Group’s recent Science Paper. Neurobiology of Learning and Memory] has suggested an alternative account of recent findings concerning very rapid systems consolidation as described in a recent paper by Tse et al [Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., & Wood, E. R., et al. (2007). Schemas and memory consolidation. Science, 316, 76–82]. This is to suppose that excitotoxic lesions of the hippocampus cause transient disruptive neural activity outside the target structure that interferes with cellular consolidation in the cortex. We disagree with this alternative interpretation of our findings and cite relevant data in our original paper indicating why this proposal is unlikely. Various predictions of the two accounts are nonetheless outlined, together with the types of experiments needed to resolve the issue of whether systems consolidation can occur very rapidly when guided by activated neural schemas.

Introduction

How does new information become incorporated into relevant frameworks of existing knowledge? What system and cellular mechanisms are involved in assimilating new information? The recent study of Tse et al. (2007), on which Rudy and Sutherland (2008) make interesting comments about the relative importance of systems and cellular consolidation, addresses this issue in the context of paired-associate learning. Using a paradigm in which rats were trained to use different flavors of food as cues to retrieve an associated spatial memory, we showed that after gradual learning (over several weeks) of a “schema” consisting of several paired-associates (PAs) involving spatial attributes, new PAs could be encoded, stored and consolidated in a single trial. Even though the task is hippocampal-dependent in the sense that new learning is blocked by lesions restricted to the hippocampus, we also observed that lesions given as soon as 48 h after the training of new PAs had no effect on subsequent memory. Lesions given 3 h after training blocked later memory. The implication seems to be that the encoding, storage and/or consolidation of new PAs is radically enhanced by prior knowledge and that systems consolidation of such information into cortex can occur much faster than has previously been observed.

Section snippets

Disruptive side-effects?

Rudy and Sutherland (2008) wonder, however, whether such unusually fast independence from the need for hippocampal processing during retrieval is really a consequence of rapid systems consolidation, or may reflect some unusual feature of our protocols. They re-plot aspects of our data for clarity, but our text may have misled them and other readers into thinking that we used a 24 h time-point for making lesions after new encoding. In fact, all lesions were either 3 or 48 h after the training of

The concept of hippocampal-dependence

It is important to stress that there are several different senses in which the learning of flavor-place PAs in this task can be said to be “hippocampal-dependent”, but other senses in which this description may seem misleading. First, the initial learning of naïve animals is impaired by hippocampal lesions that are made at the start of training (Tse et al., Fig. 1). Second, the learning of a new paired-associate schema in a new context by test-experienced animals is impaired by such lesions

Differential predictions

We have naturally wondered if there are distinct predictions that could be made based on Rudy and Sutherland’s “disruptive side-effects” and our “rapid systems-consolidation” perspectives. In our view, the key may be to finesse the side-effects of neurotoxic lesions by the alternative procedure of neural inactivation through AMPA receptor antagonists (such as CNQX), GABA agonists (such as muscimol), or even drugs that enable fast synaptic transmission but block plasticity (such as NMDA

Conclusions

While we disagree that the available data is consistent with Rudy and Sutherland’s (2008) alternative interpretation of our study, their commentary has been valuable in helping us to identify what we believe could be worthwhile follow-up experiments and in focusing on certain puzzling features of systems consolidation. Our stance, contrary to the sub-title of their piece, is that it is not “time that tells” as the defining feature of this memory process; it is the necessity for network

Acknowledgments

This commentary reflects work done under the auspices of an MRC Programme Grant and a Royal Society/Wolfson Award to R.G.M.M.

References (14)

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These authors contributed equally to this work.

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