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      Cortical Gamma Rhythms Modulate NMDAR-Mediated Spike Timing Dependent Plasticity in a Biophysical Model

      research-article
      1 , 2 , * , 1 , 2 , 3 , 4 , 1 , 2 , 5
      PLoS Computational Biology
      Public Library of Science

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          Abstract

          Spike timing dependent plasticity (STDP) has been observed experimentally in vitro and is a widely studied neural algorithm for synaptic modification. While the functional role of STDP has been investigated extensively, the effect of rhythms on the precise timing of STDP has not been characterized as well. We use a simplified biophysical model of a cortical network that generates pyramidal interneuronal gamma rhythms (PING). Plasticity via STDP is investigated at the excitatory pyramidal cell synapse from a gamma frequency (30–90 Hz) input independent of the network gamma rhythm. The input may represent a corticocortical or an information-specific thalamocortical connection. This synapse is mediated by N-methyl-D-aspartate receptor mediated (NMDAR) currents. For distinct network and input frequencies, the model shows robust frequency regimes of potentiation and depression, providing a mechanism by which responses to certain inputs can potentiate while responses to other inputs depress. For potentiating regimes, the model suggests an optimal amount and duration of plasticity that can occur, which depends on the time course for the decay of the postsynaptic NMDAR current. Prolonging the duration of the input beyond this optimal time results in depression. Inserting pauses in the input can increase the total potentiation. The optimal pause length corresponds to the decay time of the NMDAR current. Thus, STDP in this model provides a mechanism for potentiation and depression depending on input frequency and suggests that the slow NMDAR current decay helps to regulate the optimal amplitude and duration of the plasticity. The optimal pause length is comparable to the time scale of the negative phase of a modulatory theta rhythm, which may pause gamma rhythm spiking. Our pause results may suggest a novel role for this theta rhythm in plasticity. Finally, we discuss our results in the context of auditory thalamocortical plasticity.

          Author Summary

          Rhythms are well studied phenomena in many animal species. Brain rhythms in the gamma frequency range (30–90 Hz) are thought to play a role in attention and memory. In this paper, we are interested in how cortical gamma rhythms interact with information specific inputs that also have a significant gamma frequency component. The results from our computational model show that plasticity associated with learning depends on the specific frequencies of the input and cortical gamma rhythms. The results show a mechanism by which both increases and decreases in the strength of the input connection can occur, depending on the specific frequency of the input. A current mediated by NMDA receptors may be responsible for the temporal course of the plasticity seen in these brain regions. We discuss the implications of our results for conditioning paradigms applied to auditory learning.

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          Most cited references55

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          Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs.

          Activity-driven modifications in synaptic connections between neurons in the neocortex may occur during development and learning. In dual whole-cell voltage recordings from pyramidal neurons, the coincidence of postsynaptic action potentials (APs) and unitary excitatory postsynaptic potentials (EPSPs) was found to induce changes in EPSPs. Their average amplitudes were differentially up- or down-regulated, depending on the precise timing of postsynaptic APs relative to EPSPs. These observations suggest that APs propagating back into dendrites serve to modify single active synaptic connections, depending on the pattern of electrical activity in the pre- and postsynaptic neurons.
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            Competitive Hebbian learning through spike-timing-dependent synaptic plasticity.

            Hebbian models of development and learning require both activity-dependent synaptic plasticity and a mechanism that induces competition between different synapses. One form of experimentally observed long-term synaptic plasticity, which we call spike-timing-dependent plasticity (STDP), depends on the relative timing of pre- and postsynaptic action potentials. In modeling studies, we find that this form of synaptic modification can automatically balance synaptic strengths to make postsynaptic firing irregular but more sensitive to presynaptic spike timing. It has been argued that neurons in vivo operate in such a balanced regime. Synapses modifiable by STDP compete for control of the timing of postsynaptic action potentials. Inputs that fire the postsynaptic neuron with short latency or that act in correlated groups are able to compete most successfully and develop strong synapses, while synapses of longer-latency or less-effective inputs are weakened.
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              Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type.

              Q Bi, G Bi, M Poo (1998)
              In cultures of dissociated rat hippocampal neurons, persistent potentiation and depression of glutamatergic synapses were induced by correlated spiking of presynaptic and postsynaptic neurons. The relative timing between the presynaptic and postsynaptic spiking determined the direction and the extent of synaptic changes. Repetitive postsynaptic spiking within a time window of 20 msec after presynaptic activation resulted in long-term potentiation (LTP), whereas postsynaptic spiking within a window of 20 msec before the repetitive presynaptic activation led to long-term depression (LTD). Significant LTP occurred only at synapses with relatively low initial strength, whereas the extent of LTD did not show obvious dependence on the initial synaptic strength. Both LTP and LTD depended on the activation of NMDA receptors and were absent in cases in which the postsynaptic neurons were GABAergic in nature. Blockade of L-type calcium channels with nimodipine abolished the induction of LTD and reduced the extent of LTP. These results underscore the importance of precise spike timing, synaptic strength, and postsynaptic cell type in the activity-induced modification of central synapses and suggest that Hebb's rule may need to incorporate a quantitative consideration of spike timing that reflects the narrow and asymmetric window for the induction of synaptic modification.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                December 2009
                December 2009
                11 December 2009
                : 5
                : 12
                : e1000602
                Affiliations
                [1 ]Program in Neuroscience, Boston University, Boston, Massachusetts, United States of America
                [2 ]Center for Biodynamics, Boston University, Boston, Massachusetts, United States of America
                [3 ]Department of Biomedical Engineering, Boston University, Boston, Massachusetts, United States of America
                [4 ]Hearing Research Center, Boston University, Boston, Massachusetts, United States of America
                [5 ]Department of Mathematics and Statistics, Boston University, Boston, Massachusetts, United States of America
                Université Paris Descartes, Centre National de la Recherche Scientifique, France
                Author notes

                Conceived and designed the experiments: SL KS NK. Performed the experiments: SL. Analyzed the data: SL KS NK. Wrote the paper: SL KS NK.

                Article
                09-PLCB-RA-0791R2
                10.1371/journal.pcbi.1000602
                2782132
                20011119
                131253f9-d377-4579-aaaa-9d4b7237ee31
                Lee et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 2 July 2009
                : 9 November 2009
                Page count
                Pages: 13
                Categories
                Research Article
                Neuroscience
                Neuroscience/Sensory Systems
                Neuroscience/Theoretical Neuroscience

                Quantitative & Systems biology
                Quantitative & Systems biology

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