Intrinsic volatility of synaptic connections — a challenge to the synaptic trace theory of memory

doi:10.1016/j.conb.2017.06.006

Current Opinion in Neurobiology

Volume 46, October 2017, Pages 7-13

https://doi.org/10.1016/j.conb.2017.06.006 Get rights and content

Highlights

•
Learning induces synaptic re-organization of cortical circuits.
•
Substantial synaptic re-organization also occurs spontaneously.
•
It is unclear what elements provide stability necessary for memory maintenance.
•
Different mechanisms at synaptic to local network level can safeguard memories.

According to the synaptic trace theory of memory, activity-induced changes in the pattern of synaptic connections underlie the storage of information for long periods. In this framework, the stability of memory critically depends on the stability of the underlying synaptic connections. Surprisingly however, synaptic connections in the living brain are highly volatile, which poses a fundamental challenge to the synaptic trace theory. Here we review recent experimental evidence that link the initial formation of a memory with changes in the pattern of connectivity, but also evidence that synaptic connections are considerably volatile even in the absence of learning. Then we consider different theoretical models that have been put forward to explain how memory can be maintained with such volatile building blocks.

Section snippets

Synapses and memory

A needle that punctures a cloth leaves a small mark, making it easier to re-puncture that point. René Descartes, the 17th century philosopher, mathematician and scientist used this metaphor (see Figure 1a) to explain his theory of memory that was based on animal spirits flowing through pores in the brain [1]. This theory is long obsolete. However, the metaphor still nicely captures the very essence of the contemporary synaptic trace theory of memory. Today, it is generally believed that

Synaptic volatility challenges the synaptic trace theory

If a specific pattern of connectivity is the physical basis of long term memory, then our ability to retrieve this memory after years, and even decades, crucially entails that this pattern remains stable. Surprisingly however, cortical spines are being constantly formed and eliminated in the living brain, implying that the corresponding synapses are highly volatile (Figure 2a,b). For example, a recent study suggested that within several weeks, the synaptic network in the hippocampus CA1 region

Memory in the presence of synaptic volatility

In the remainder of this review we will consider three types of solutions that have been proposed to explain how functional stability is maintained in a volatile brain. We will focus on synaptic mechanisms, bearing in mind the possibility that stable, non-synaptic elements may also contribute to the storage of information for long periods [45, 46].

One explanation to the apparent discrepancy between the timescales of synaptic turnover and the timescales of memory maintenance is — that there is

Concluding remarks

Here we reviewed some of the recent evidence supporting the synaptic trace theory of memory. This theory agrees with our everyday intuition that information is stored for long-periods of time in elements that are physically as stable as possible, be it an inscription on an obelisk or the needle marks in Descartes’ cloth. Yet, we pointed out a substantial challenge to this theory, the fact that the ‘stable’ elements of this theory — the synapses, are in fact highly volatile. We discussed some

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

This work was supported by the Israel Science Foundation (Grant No. 757/16), the DFG (CRC 1080) and by the Gatsby Charitable Foundation. We thank David Hansel, Noam Ziv and Haruo Kasai for carefully reading the manuscript and helpful comments and Zehava Cohen for help in preparing Figure 1.

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View full text

Intrinsic volatility of synaptic connections — a challenge to the synaptic trace theory of memory

Highlights

Section snippets

Synapses and memory

Synaptic volatility challenges the synaptic trace theory

Memory in the presence of synaptic volatility

Concluding remarks

Conflict of interest statement

References and recommended reading

Acknowledgements

J Physiol

Neuron

Sci Rep

PLoS Biol

Curr Opin Neurobiol

Neuron

Nat Neurosci

PLoS Biol

Neuron

PLoS Comput Biol

PLoS Comput Biol

PLoS Comput Biol

PLOS ONE

J Neurosci

L'homme, et la formation du foetus

What is memory? The present state of the engram

BMC Biol

In search of the engram

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Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning

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PV plasticity sustained through D1/5 dopamine signaling required for long-term memory consolidation

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