Matching storage and recall: hippocampal spike timing–dependent plasticity and phase response curves


Hippocampal area CA3 is widely considered to function as an autoassociative memory. However, it is insufficiently understood how it does so. In particular, the extensive experimental evidence for the importance of carefully regulated spiking times poses the question as to how spike timing–based dynamics may support memory functions. Here, we develop a normative theory of autoassociative memory encompassing such network dynamics. Our theory specifies the way that the synaptic plasticity rule of a memory constrains the form of neuronal interactions that will retrieve memories optimally. If memories are stored by spike timing–dependent plasticity, neuronal interactions should be formalized in terms of a phase response curve, indicating the effect of presynaptic spikes on the timing of postsynaptic spikes. We show through simulation that such memories are competent analog autoassociators and demonstrate directly that the attributes of phase response curves of CA3 pyramidal cells recorded in vitro qualitatively conform with the theory.

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Figure 1: Normative theory of spike timing–based autoassociative memory.
Figure 2: Quality of memory retrieval in an optimally constructed spike timing–based autoassociative memory model: numerical simulations.
Figure 3: Experimental measurement of the PRC in CA3 hippocampal neurons.
Figure 4: Effect of EPSG amplitude on the PRC.


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We thank B. Gutkin, D. MacKay and E. Shea-Brown for valuable discussions and E.O. Mann and D. McLelland for their help with Igor procedures. This work was supported by the Gatsby Charitable Foundation (M.L., P.D.), the European Bayesian-Inspired Brain and Artefacts project (M.L., P.D.), the Biotechnology and Biological Sciences Research Council (J.K., O.P.), the Kwanjung Educational Foundation, Korea (J.K.) and the Oxford University Clarendon Fund (J.K.).

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Correspondence to Máté Lengyel.

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Supplementary information

Supplementary Fig. 1

Recall performance in adversarial settings. (PDF 185 kb)

Supplementary Fig. 2

Consequences of a broad, smoothly varying STDP curve on the optimal coupling function and phase response curves. (PDF 165 kb)

Supplementary Fig. 3

Effect of increased oscillatory frequency on the PRC. (PDF 359 kb)

Supplementary Fig. 4

Burst-based PRCs. (PDF 448 kb)

Supplementary Methods (PDF 29 kb)

Supplementary Note (PDF 76 kb)

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Lengyel, M., Kwag, J., Paulsen, O. et al. Matching storage and recall: hippocampal spike timing–dependent plasticity and phase response curves. Nat Neurosci 8, 1677–1683 (2005).

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