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Role of experience and oscillations in transforming a rate code into a temporal code

Abstract

In the vast majority of brain areas, the firing rates of neurons, averaged over several hundred milliseconds to several seconds, can be strongly modulated by, and provide accurate information about, properties of their inputs. This is referred to as the rate code. However, the biophysical laws of synaptic plasticity require precise timing of spikes over short timescales (<10 ms)1,2. Hence it is critical to understand the physiological mechanisms that can generate precise spike timing in vivo, and the relationship between such a temporal code and a rate code. Here we propose a mechanism by which a temporal code can be generated through an interaction between an asymmetric rate code and oscillatory inhibition. Consistent with the predictions of our model, the rate3,4 and temporal5,6,7 codes of hippocampal pyramidal neurons are highly correlated. Furthermore, the temporal code becomes more robust with experience. The resulting spike timing satisfies the temporal order constraints of hebbian learning. Thus, oscillations and receptive field asymmetry may have a critical role in temporal sequence learning.

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Figure 1: Hippocampal spatio-temporal receptive fields.
Figure 2: A mechanism that can generate a temporal code from a rate code.
Figure 3: Relationship between hippocampal rate and temporal codes.
Figure 4: Experience dependence of the temporal code.

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Acknowledgements

We thank W.F. Asaad, G. Liu, K. Louie, J. Raymond and S. Schnall for comments on the manuscript. This work was supported by the NIH (M.A.W.) and an HHMI pre-doctoral fellowship (A.K.L.). Parts of this work were presented at the Computational Neuroscience Meeting 2000 and at the Society for Neuroscience meeting 2001.

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Correspondence to M. R. Mehta or M. A. Wilson.

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Mehta, M., Lee, A. & Wilson, M. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417, 741–746 (2002). https://doi.org/10.1038/nature00807

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