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The Journal of Neuroscience, October 6, 2004, 24(40):8873-8884; doi:10.1523/JNEUROSCI.2661-04.2004

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Cellular/Molecular
Timing and Balance of Inhibition Enhance the Effect of Long-Term Potentiation on Cell Firing

Carrie P. Marder and Dean V. Buonomano

Departments of Neurobiology and Psychology and Brain Research Institute, University of California, Los Angeles, Los Angeles, California 90095

The role of a neuron in neural processing is ultimately determined by whether or not it fires an action potential in a given context. Studies on synaptic plasticity have focused primarily on changes in EPSPs, and not on whether plasticity translates into changes in firing. However, this issue has been addressed by examining EPSP-spike (E-S) potentiation, which enhances the ability of an EPSP of a fixed slope to elicit spikes after long-term potentiation (LTP). Although LTP is thought to underlie learning and memory, E-S potentiation could play an equally important role by potentiating the neuronal input-output function. Here, we used a combined experimental and theoretical approach to examine both the mechanisms underlying E-S potentiation as well as the role of inhibition in shaping the input-output function of neurons. Whereas previous studies examined tetanus-LTP, in which inhibitory synapses may have undergone plasticity, here we examined pairing-induced associative LTP. We determined that although intact inhibition was necessary for pairing-induced E-S potentiation, inhibitory plasticity was not. We further established using computer simulations that a primary mechanism of E-S potentiation was a change in the relative recruitment and latency of inhibitory neurons. Although these studies do not exclude the presence of additional mechanisms of E-S potentiation that may be engaged depending on the induction protocol, they do establish that under intact pharmacology, LTP of the Schaffer collateral to CA1 pyramidal neuron synapses will produce E-S potentiation as a result of changes in the balance and timing of excitation and inhibition.

Key words: hippocampus; CA1; inhibition; EPSP-spike potentiation; long-term potentiation; network; input-output

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Received Jan 16, 2004; revised August 26, 2004; accepted August 28, 2004.

This article has been cited by other articles:

				A. E. Fink and T. J. O'Dell Short Trains of Theta Frequency Stimulation Enhance CA1 Pyramidal Neuron Excitability in the Absence of Synaptic Potentiation J. Neurosci., September 9, 2009; 29(36): 11203 - 11214. [Abstract] [Full Text] [PDF]

				E. Campanac and D. Debanne Spike timing-dependent plasticity: a learning rule for dendritic integration in rat CA1 pyramidal neurons J. Physiol., February 1, 2008; 586(3): 779 - 793. [Abstract] [Full Text] [PDF]

				J. S. Haas, T. Nowotny, and H.D.I. Abarbanel Spike-Timing-Dependent Plasticity of Inhibitory Synapses in the Entorhinal Cortex J Neurophysiol, December 1, 2006; 96(6): 3305 - 3313. [Abstract] [Full Text] [PDF]

				D. V. Buonomano A Learning Rule for the Emergence of Stable Dynamics and Timing in Recurrent Networks J Neurophysiol, October 1, 2005; 94(4): 2275 - 2283. [Abstract] [Full Text] [PDF]

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