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Neuron. 2017 Sep 27;96(1):177-189.e7. doi: 10.1016/j.neuron.2017.09.021.

Synaptic Transmission Optimization Predicts Expression Loci of Long-Term Plasticity.

Author information

1
Centre for Neural Circuits and Behaviour, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK. Electronic address: rui.costa@cncb.ox.ac.uk.
2
Department of Pharmacology, University of Oxford, Oxford, UK.
3
Skirball Institute, Neuroscience Institute, Departments of Otolaryngology, Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA.
4
Skirball Institute, Neuroscience Institute, Departments of Otolaryngology, Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA; Center for Neural Science, New York University, New York, NY, USA; Howard Hughes Medical Institute Faculty Scholar.
5
Centre for Neural Circuits and Behaviour, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK.

Abstract

Long-term modifications of neuronal connections are critical for reliable memory storage in the brain. However, their locus of expression-pre- or postsynaptic-is highly variable. Here we introduce a theoretical framework in which long-term plasticity performs an optimization of the postsynaptic response statistics toward a given mean with minimal variance. Consequently, the state of the synapse at the time of plasticity induction determines the ratio of pre- and postsynaptic modifications. Our theory explains the experimentally observed expression loci of the hippocampal and neocortical synaptic potentiation studies we examined. Moreover, the theory predicts presynaptic expression of long-term depression, consistent with experimental observations. At inhibitory synapses, the theory suggests a statistically efficient excitatory-inhibitory balance in which changes in inhibitory postsynaptic response statistics specifically target the mean excitation. Our results provide a unifying theory for understanding the expression mechanisms and functions of long-term synaptic transmission plasticity.

KEYWORDS:

endocannabinoids; excitation-inhibition balance; expression loci; inhibitory plasticity; long-term synaptic plasticity; nitric oxide; retrograde messengers; synaptic transmission; theory

PMID:
28957667
PMCID:
PMC5626823
DOI:
10.1016/j.neuron.2017.09.021
[Indexed for MEDLINE]
Free PMC Article

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